Abstract

We used functional magnetic resonance imaging and a 1-back task to assess working memory (WM) for spatial (sound location) and nonspatial (sound category) auditory information in younger and older adults. A mixed block–event-related design was used to measure sustained activity during each task block and transient activity to targets (repetitions of location or category). In both groups, there was increased sustained activity for category WM in left anterior temporal cortex and inferior prefrontal cortex (PFC) and increased activity for location WM in right inferior parietal cortex and dorsal PFC. There were no reliable age differences in this pattern of activity. Older adults had more sustained activity than younger adults in left PFC during both tasks, suggesting that additional PFC recruitment in older adults reflects nonspecific engagement of frontally mediated task-monitoring processes. Both groups showed lower transient than sustained activity in auditory cortex bilaterally; however, older adults showed smaller target-related reductions of activity during the category task. A greater reduction of activity to category targets in left auditory cortex was associated with better performance on this task in older adults, suggesting that a failure to modulate activity appropriately when a stimulus is repeated, or when a particular feature of the stimulus is repeated, could lead to reduced ability to detect this repetition.

Introduction

An influential discovery about the functional organization of the primate visual system was that the processing of object identity, or “what,” and object location, that is “where,” is functionally separated along specialized ventral and dorsal cortical pathways, respectively (Ungerleider and Mishkin 1982). This has been repeatedly demonstrated in studies of patients with ventral occipitotemporal or dorsal parietal lesions (e.g., Holmes 1918; Damasio et al. 1982; Petersen et al. 1989; Ogden 1993; Goodale 1996; Moscovitch et al. 1997) and in monkeys with similar resections of tissue (e.g., Desimone and Ungerleider 1989). Functional neuroimaging studies in humans also have shown this ventral/dorsal distinction of visual processing using tasks of perception (Haxby et al. 1994), episodic memory (Moscovitch et al. 1995), and working memory (WM) (Courtney et al. 1996, 1998).

Less is known about the organization of the auditory system for processing sound identity and location, but recent work has provided strong evidence of a similar dissociation in this sensory modality. For example, evidence from recent studies in nonhuman primates suggests that auditory scene analysis may be carried out by at least 2 functionally specialized processing streams. The stream representing sound identity involves rostral auditory cortex and inferior frontal regions, whereas processing of sound location depends on caudal auditory cortex and dorsal prefrontal cortex (PFC) (Romanski et al. 1999; Rauschecker and Tian 2000). Human lesion data suggest a similar dissociation of areas subserving identification and localization. Damage to the anterior and middle portions of the temporal lobe impair recognition of environmental sounds, voices, or melodies (Rosati et al. 1982; Peretz et al. 1994; Schnider et al. 1994; Clarke et al. 2000), and lesions in posterior temporal and parietal areas result in localization deficits (Shankweiler 1961; Bisiach et al. 1984; Clarke et al. 2000) and auditory neglect (De Renzi et al. 1989; Vallar et al. 1995).

Although functional neuroimaging studies in the auditory domain are less numerous than visual studies, they also support the idea of separate processing streams for audition. Regions in temporal cortex anterior to Heschl's gyrus are activated for meaningful and complex sounds such as human vocal sounds and environmental sounds (Belin et al. 2000), whereas posterior temporal cortex and/or parietal regions are active during auditory localization tasks (Bushara et al. 1999; Weeks et al. 1999), particularly when multiple sound sources have to be processed (Zatorre et al. 2002). Direct comparisons between auditory identification and localization have shown separate processing streams similar to those identified in monkeys (Alain et al. 2001; Maeder et al. 2001; Rama et al. 2004; Arnott et al. 2005). These studies reported increased activity in anterior temporal and inferior frontal cortices for processing sound identity, whereas sound localization recruited areas that were primarily distributed in dorsal regions, including parietal and frontal regions.

Normal aging is associated with important changes in cognitive functions, which are paralleled by changes in brain function. For instance, older adults show more activation of dorsolateral PFC than do younger adults during both visual identification and localization tasks (Grady et al. 1994), consistent with the increased recruitment of frontal regions reported in older adults across a broad spectrum of visual tasks (Cabeza et al. 1997; Grady et al. 1998; Madden et al. 1999; Reuter-Lorenz et al. 2000; Grady 2002; Morcom et al. 2003). However, healthy aging does not disrupt the functional dissociation of the ventral and dorsal visual processing pathways in posterior cortices (Grady et al. 1994). These results suggest that perceptual mechanisms, including those for visual identification and localization, are largely intact in posterior regions, but older adults frequently engage somewhat different cognitive processes compared with younger adults, accounting for the frontal differences. This may reflect an age-related shift in the cognitive resources utilized with age to greater reliance on those involved in executive and monitoring functions, as well as a recruitment of these frontally mediated processes at lower levels of task load in older adults (Grady et al. 1998, 2003; Grady 2002). In some experiments, this additional recruitment of PFC is accompanied by better task performance (Cabeza et al. 2002; Grady et al. 2003), suggesting that it serves a compensatory function.

Most of the studies done to date comparing brain activity in younger and older adults have utilized visual tasks and none have addressed the question of whether there are age differences in the processing of spatial and nonspatial information in the auditory system. The purpose of the current experiment was to examine the effects of aging on auditory WM for spatial (sound location) and nonspatial (sound category) features of environmental sounds using 1-back tasks and functional magnetic resonance imaging (fMRI). Because older adults often show worse performance on WM tasks compared with younger adults (e.g., Babcock and Salthouse 1990; Foos and Wright 1992; Park et al. 2002), including auditory WM tasks (Raz et al. 1989; Pichora-Fuller et al. 1995; Takakura et al. 2003), we attempted to match performance between groups on these tasks to remove the influence of performance ability on differences in brain activity. We hypothesized that both younger and older adults would show a ventral/dorsal dissociation in brain activity during these sound identity and localization tasks, respectively. We also expected that the older adults would have additional recruitment of PFC during both tasks, as was found earlier for the visual system (Grady et al. 1994). In addition, we used a mixed event-related–block design, which allowed us to examine both sustained activity throughout spatial and nonspatial blocks and transient activity to targets (i.e., repetitions of category or location). Current concepts of how PFC participates in WM emphasize its role in executive functions, such as monitoring and inhibition (for a review, see D'Esposito and Postle 2002). If these are the kinds of cognitive process that older adults recruit to a greater extent than do younger adults, it seems likely that such mechanisms would be engaged throughout the period of task performance and thus would be seen as additional PFC recruitment during sustained activity on these 1-back tasks. On the other hand, whatever differentiates younger and older adults in the decision to respond to a target, or in the sensorimotor aspects of the response itself, will be reflected in age differences in transient activity.

Materials and Methods

A total of 18 younger adults and 21 older adults participated in the experiment. Data from 2 younger adults and 3 older adults had to be discarded because of excessive head motion or other technical difficulties, resulting in a final sample of 16 younger (mean age = 26.1 ± 3.7 years; 8 men) and 18 older adults (mean age = 65.8 ± 4.5 years; 9 men). All were right handed and screened using a detailed health questionnaire to exclude health problems and/or medications that might affect cognitive function and brain activity, including strokes and cardiovascular disease. The structural magnetic resonance imagings (MRIs) also were inspected to rule out severe white matter abnormalities. The younger adults had slightly more years of education than did the older adults (young, M = 18.2 ± 2.3 years; old, M = 16.1 ± 2.5 years; t32 = 2.5, P < 0.05). Participants came into the laboratory prior to scanning for hearing tests and received practice on the WM tests to increase the likelihood that performance during the scans would be matched in younger and older adults. All participants achieved a criterion of at least 90% correct on both WM tests in this prescanning session. All gave informed consent for their participation, following the guidelines of the Research Ethics Board at Baycrest and the University of Toronto.

The stimuli used in this experiment were environmental sounds from 3 semantic categories: human (nonspeech) sounds, animal sounds, and sounds made by musical instruments. In each category, 10 different exemplars were chosen from a larger data bank, and pilot testing confirmed that all stimuli included in the study could be unambiguously categorized. Stimuli were edited to have a duration of 1005 ms, and onsets and offsets were shaped by 2 halves of an 8-ms Kaiser window, respectively. Stimuli were digitally generated with 16-bit resolution and a 12.21-kHz sampling rate, then passed through a digital-to-analog converter (Tucker-Davis Technology, Gainesville, FL). The sounds were delivered to the listener at about 88 dB sound pressure level (root-mean square) by means of circumaural, fMRI-compatible headphones (Avotec, Jensen Beach, FL), acoustically padded to suppress scanner noise by 25 dB. Presentation occurred at 3 possible azimuth locations relative to straight ahead (−90°, 0°, +90°) using head-related transfer functions that represent the acoustic effects of the head and ears of an average listener (Wenzel et al. 1993).

Participants performed 1-back tasks in which sound identity or sound location was occasionally repeated. Prior to a block of trials, participants were presented with a visual prompt word (e.g., location or category) on a screen indicating target type. This prompt appeared on the screen 10 s prior to the first sound and remained on for the duration of the task block. The location task required participants to press a button as quickly as possible whenever a stimulus occurred at the same location as the preceding sound, regardless of sound identity. In the category task, participants were instructed to respond whenever a category (animal, human, music) was repeated regardless of the location. Aside from the cue, the set of stimuli used was identical in both the category and location tasks. Participants' responses were registered using an fMRI-compatible response pad (Lightwave Technologies, Surrey, BC, Canada). Participants performed each designated task for 30 s followed by a 20-s baseline in which no stimuli were presented. This on/off sequence was repeated 6 times in each scanning run, and 6 runs were performed in total. During the tasks, the stimulus onset asynchrony was 2 s and the intertarget intervals varied between 4 and 12 s. The tasks alternated throughout each fMRI run, and the order of the tasks was counterbalanced within and across participants. Participants kept their eyes open throughout all scans.

Images were acquired with a General Electric Signa 3-T magnet at Sunnybrook Health Science Centre. We first obtained a T1-weighted anatomical volume using spoiled gradient echo recall (time echo [TE] = 3.4 ms, time repetition [TR] = 35 ms, flip angle = 35) for coregistration with the functional images and to ensure that there were no significant brain abnormalities in any of the participants. T2* functional images (TE = 40 ms, TR = 2000 ms, flip angle =80) were obtained using single-shot spiral in–out acquisition (Glover and Lai 1998; Preston et al. 2004). Each functional sequence consisted of 25 5-mm thick axial slices, positioned to image the whole brain. The participant's head was restrained using a vacuum pillow that fit inside the head coil.

Data preprocessing and analysis were carried out using the Analysis of Functional Images software package (Cox 1996; Cox and Hyde 1997). The first 10 time points in each run were excluded from all analyses to remove those images where transient signal changes occurred as brain magnetization reached a steady state. In the preprocessing stage, time series data were detrended using a linear function and spatially coregistered to correct for head motion using a 3-dimensional Fourier transform interpolation to a reference image acquired during the scanning session. The peak range of head motion was less than 1.5 mm for all participants. The coregistration results also were checked visually for additional quality control.

We used the general linear model (GLM) to analyze the fMRI data. Sustained and event-related effects both were coded in the GLM using canonical hemodynamic response functions (HRFs). For sustained activity, the shape of the HRF was modeled as a “gamma” function convolved with a boxcar function of width equal to the duration of the block. For transient event-related activity, we also used a gamma function time locked on target onset. Only correct trials were included in the event-related analysis. This approach allowed us to assess activity simultaneously in blocks and events after removing the effect of each on the other (Donaldson et al. 2001). The activation maps created by the GLMs for each condition and each participant were then transformed into stereotaxic space (Cox 1996) and spatially smoothed using a Gaussian filter with a full-width half-maximum value of 6.0 mm. These last 2 steps were performed to facilitate the within- and between-group analyses, which consisted of voxel-wise, mixed-effects (conditions fixed, participants random) analyses of variance (ANOVAs) with condition (sustained and transient activity during location and category tasks) as within-subject factors. Separate ANOVAs were carried out within both groups to examine 1) differences in sustained activity between location and category tasks, 2) differences in transient activity between tasks, and 3) differences between sustained and transient activity for each task. An additional ANOVA was carried out to determine differences between the young and old groups in brain activity. For all of these contrasts, we used a statistical threshold of P < 0.001 (uncorrected) and a cluster size of 300 μL (6 original voxels). In addition, for each region showing a difference in activity between tasks or groups, we ensured that the region also showed a significant change in activity compared with the baseline (either an increase or a decrease) in one or both groups (P < 0.005).

Results

Behavioral Results

Figure 1 shows the group mean accuracy and response times (RTs) of younger and older adults on the WM tasks. There were significant effects of both task, F1,32 = 7.5, P = 0.01, and group, F1,32 = 24.6, P < 0.001, on accuracy of target detection. However, these main effects were qualified by a significant interaction of task and group, F1,32 = 16.1, P < 0.001. t-tests comparing the 2 groups on the category and location tasks separately showed that older adults detected significantly fewer category targets than did younger adults, t32 = 7.8, P < 0.001. In contrast, there was no reliable difference between groups on the location task, t32 = 1.7, P > 0.05. Younger adults showed no difference in performance between the category and location tasks, t15 = 1.9, P > 0.05, whereas the older adults detected significantly fewer targets in the category task than in the location task, t17 = 3.8, P < 0.01.

Figure 1.

Performance on the category and location WM tasks in younger and older adults. Error bars represent the standard deviation.

Figure 1.

Performance on the category and location WM tasks in younger and older adults. Error bars represent the standard deviation.

There was a significant effect of task on RT, F1,32 = 56.9, P < 0.001, with both groups showing slower RTs on the category task relative to the location task (Fig. 1). The main effect of group also was reliable, F1,32 = 4.2, P < 0.05, and the interaction of task and group was almost significant, F1,32 = 3.9, P = 0.06. Although the interaction was not significant, we carried out t-tests comparing RT from the 2 groups on category and location separately, as the pattern appeared to be similar to that seen for accuracy. Indeed, older adults performed significantly slower on the category task, t32 = 2.7, P < 0.02, whereas older adults' RT on the location task was not significantly different from that seen in the younger group, t32 = 1.3, P > 0.05. These behavioral results indicate that our pretesting of participants prior to scanning ensured that the 2 groups performed equally well on the location task, but carrying out the category task in the MRI environment adversely affected the older adults' performance on this task.

fMRI Results—Task Effects

The differences in sustained activity between category and location tasks were similar in younger and older adults (Fig. 2 and Table 1). Both groups showed more sustained activity for the category than the location task in the left anterior temporal cortex, the left inferior and middle frontal gyri, and a region in medial PFC that was likely the presupplementary motor area (Petit et al. 1998). Both groups had significantly more sustained activity for location WM, relative to category, in dorsal PFC, precentral gyrus, the superior parietal lobule, and the inferior parietal lobule (IPL), all in the right hemisphere. In all of these regions with differences between the WM tasks, there also was more sustained activity during the task relative to baseline.

Figure 2.

Task differences in sustained activity for younger and older adults (from within-group ANOVAs) are shown on the average structural images for each group. Red indicates greater activity for category and blue indicates greater activity for the location task. Clusters shown are thresholded at P < 0.001 and contain at least 300 μL.

Figure 2.

Task differences in sustained activity for younger and older adults (from within-group ANOVAs) are shown on the average structural images for each group. Red indicates greater activity for category and blue indicates greater activity for the location task. Clusters shown are thresholded at P < 0.001 and contain at least 300 μL.

Table 1

Sustained activity during category and location tasks in both groups

Gyrus or region Hem BA Younger adults Older adults 
   x y z x y z 
Category > location         
    Inferior frontal 45 −38 28 14 −42 23 
    Middle frontal −46 17 29 −46 19 27 
    Medial frontal −3 55 −2 11 56 
    Middle temporal 21/22 −54 −29 −51 −9 −8 
Location > category         
    Middle frontal 22 −12 57 25 −11 51 
    Precentral 54 13 43 15 
    Inferior parietal 40 42 −45 37 50 −46 46 
    Superior parietal −67 54 −68 50 
Gyrus or region Hem BA Younger adults Older adults 
   x y z x y z 
Category > location         
    Inferior frontal 45 −38 28 14 −42 23 
    Middle frontal −46 17 29 −46 19 27 
    Medial frontal −3 55 −2 11 56 
    Middle temporal 21/22 −54 −29 −51 −9 −8 
Location > category         
    Middle frontal 22 −12 57 25 −11 51 
    Precentral 54 13 43 15 
    Inferior parietal 40 42 −45 37 50 −46 46 
    Superior parietal −67 54 −68 50 

Note: All P's < 0.001. Clusters are ≥300 μL and also show significant (P < 0.005) increase in task versus baseline. Hem = hemisphere; BA = Brodmann's area; L = left; R = right. x (right/left): negative values are in the left hemisphere; y (anterior/posterior): negative values are posterior to the zero point (located at the anterior commissure); z (superior/inferior): negative values are inferior to the plane defined by the anterior and posterior commissures.

There were fewer task differences in target-related transient activity than for sustained activity (Table 2). Younger adults had more activity for category targets, relative to location targets, in a region of the right precentral gyrus, whereas older adults had more activity for category targets in a number of regions. These included bilateral inferior parietal cortex and a medial frontal region (Table 2). Neither group showed reliably greater activity for location targets relative to category targets.

Table 2

Target-related transient activity (category > location)

Gyrus or region Hem BA x y z 
Younger adults      
    Precentral 44 11 
Older adults      
    Medial frontal −7 −6 49 
    Inferior parietal 40 −55 −35 27 
 40 −33 −42 45 
 40 37 −45 42 
Gyrus or region Hem BA x y z 
Younger adults      
    Precentral 44 11 
Older adults      
    Medial frontal −7 −6 49 
    Inferior parietal 40 −55 −35 27 
 40 −33 −42 45 
 40 37 −45 42 

Note: All clusters are ≥300 μL, P < 0.001. All clusters have significantly (P < 0.005) increased activity during targets compared with baseline. Hem = hemisphere; BA = Brodmann's area; L = left; R = right. x (right/left): negative values are in the left hemisphere; y (anterior/posterior): negative values are posterior to the zero point (located at the anterior commissure); z (superior/inferior): negative values are inferior to the plane defined by the anterior and posterior commissures.

The final set of within-group contrasts examined differences between sustained activity and transient target-related activity for the 2 tasks (Fig. 3 and Table 3). Both young and old adults had more sustained than transient activity in bilateral auditory cortex during both tasks. This reduction in activity due to detection of category and location repeats is similar to the reduction seen for stimulus repeats, termed magnetic resonance (MR) adaptation by Grill-Spector and Malach (2001). More sustained activity during the category and location tasks also was seen in the left inferior frontal gyrus. Greater sustained than transient activity during the location task in both groups was seen in the right inferior frontal gyrus (Fig. 3b). Conversely, both age groups had greater transient activity, compared with sustained, in a number of regions, including medial portions of the frontal and parietal lobes, during both tasks. In addition, both groups had more transient activity for category targets in the insula bilaterally and left IPL and for the location task in the right parahippocampal gyrus (Table 3). In all of these regions with a sustained-transient difference, there was a significant increase of activity in the condition of interest versus baseline, with one exception. This exception was the right parahippocampal gyrus in young adults, which showed more transient than sustained activity during the location task due to a decrease in sustained activity, rather than an increase in transient activity.

Figure 3.

Differences between sustained and transient activity for both groups are shown on the average structural images for each group (from within-group ANOVAs) for the category task (a) and the location task (b). Red indicates greater transient activity for targets and blue indicates greater sustained activity. Clusters shown are thresholded at P < 0.001 and contain at least 300 μL.

Figure 3.

Differences between sustained and transient activity for both groups are shown on the average structural images for each group (from within-group ANOVAs) for the category task (a) and the location task (b). Red indicates greater transient activity for targets and blue indicates greater sustained activity. Clusters shown are thresholded at P < 0.001 and contain at least 300 μL.

Table 3

Contrasts of sustained and transient activity during category and location tasks common to both groups

Gyrus or region Hem BA Younger adults Older adults 
   x y z x y z 
Category: sustained > transient         
    Inferior frontal 44 −40 34 −44 30 
 45 −27 22 11 −36 26 15 
    Medial frontal −3 56 −1 51 
    Superior temporal 22 −53 −21 −63 −39 
 22 49 −9 49 −30 
Category: transient > sustained         
    Medial frontal  42 21 38 19 
    Posterior cingulate  31 −33 38 −1 −28 38 
    Inferior parietal 40 −34 −40 58 −40 −34 54 
    Insula  −42 −3 17 −40 −3 10 
  36 12 40 −3 10 
Location: sustained > transient         
    Inferior frontal 45 −33 21 22 −31 22 13 
 45 30 23 10 30 27 
 9/44 51 34 48 28 
 9/44 −42 31 −41 28 
    Superior temporal 22 −52 −23 10 −52 −44 
 22 50 −8 57 −21 
Location: transient > sustained         
    Anterior cingulate 32 43 10 −1 54 
    Posterior cingulate  31 −37 38 −25 35 
    Parahippocampusa 36 21 −36 −14 26 −38 −13 
Gyrus or region Hem BA Younger adults Older adults 
   x y z x y z 
Category: sustained > transient         
    Inferior frontal 44 −40 34 −44 30 
 45 −27 22 11 −36 26 15 
    Medial frontal −3 56 −1 51 
    Superior temporal 22 −53 −21 −63 −39 
 22 49 −9 49 −30 
Category: transient > sustained         
    Medial frontal  42 21 38 19 
    Posterior cingulate  31 −33 38 −1 −28 38 
    Inferior parietal 40 −34 −40 58 −40 −34 54 
    Insula  −42 −3 17 −40 −3 10 
  36 12 40 −3 10 
Location: sustained > transient         
    Inferior frontal 45 −33 21 22 −31 22 13 
 45 30 23 10 30 27 
 9/44 51 34 48 28 
 9/44 −42 31 −41 28 
    Superior temporal 22 −52 −23 10 −52 −44 
 22 50 −8 57 −21 
Location: transient > sustained         
    Anterior cingulate 32 43 10 −1 54 
    Posterior cingulate  31 −37 38 −25 35 
    Parahippocampusa 36 21 −36 −14 26 −38 −13 

Note: Clusters have P < 0.001 and are ≥300 μL. All areas have increased activity compared with baseline (P < 0.005) unless otherwise indicated. Hem = hemisphere; BA = Brodmann's area; L = left; R = right. x (right/left): negative values are in the left hemisphere; y (anterior/posterior): negative values are posterior to the zero point (located at the anterior commissure); z (superior/inferior): negative values are inferior to the plane defined by the anterior and posterior commissures.

a

Region in young adults had significantly decreased sustained activity (P < 0.001) during the location task.

fMRI Results—Age Effects

Though there appeared to be some differences in the exact regions where younger and older adults had task-related modulations of sustained activity differentiating category and location WM (see Fig. 2), there were no reliable age differences in these brain regions or in any other areas (even when the statistical threshold was lowered to P < 0.005). There also were no group differences in the regions that differentiated category from location targets (Table 2). Overall, this lack of group differences in the contrasts between the category and location tasks suggests that the dissociations between ventral and dorsal auditory streams were equivalent in the younger and older adults.

However, there was a significant main effect of age group on brain activity in a number of regions, all of which showed more activity in the older adults. Inspection of the group difference in these regions indicated that in many of them the age effect was more robust for sustained than for transient activity. To examine these age differences in more detail, we contrasted activity in young versus old adults for sustained and transient conditions in each task separately. We then carried out a conjunction analysis to identify those areas with more activity in older adults in sustained activity for both tasks, in transient activity for both tasks, and whether there were any areas with more activity in older adults across all 4 conditions. For these analyses, we used a threshold of P < 0.005 for each contrast entering into the conjunction. In addition to identifying overlapping areas of group difference, this analysis also indicated areas with a group difference in only one of the conditions.

Figure 4 shows the results of this analysis for sustained activity. Older adults had more sustained activity than younger adults in a number of areas in both category and location tasks, notably left inferior PFC and IPL, bilateral extrastriate regions, and bilateral putamen (Fig. 4a and Table 4). Older adults also had more sustained activity during the category task in right inferior PFC (x = 36, y = 33, z = 7, P < 0.001), right dorsolateral PFC (x = 35, y = 30, z = 37, P < 0.001), and medial PFC (x = −3, y = 26, z = 40, P < 0.001). During the location task, older adults showed more sustained activity than did the younger adults in left superior parietal cortex (x = −24, y = −47, z = 50, P < 0.001, Fig. 4a). In most of these regions, including the left inferior PFC (see Fig. 4b), the group difference in activity was due to significantly increased activity relative to baseline in the older adults. However, 4 regions showed a group difference primarily because of reduced activity versus baseline in the younger adults. These areas were the right and left fusiform gyri, the paracentral lobule, and the left IPL (Fig. 4c).

Figure 4.

(a) Areas with more sustained activity in older adults are shown on the average structural image of all participants. Colored regions indicate areas where older adults had more sustained activity than younger adults during the category task (blue), the location task (red), or both tasks (yellow). All images entered into the conjunction analysis had P < 0.005. Activity versus baseline in the left PFC region (circled) is shown in (b), and activity for left IPL (circled) is shown in (c). Asterisks located above columns indicate that activity is significantly different from baseline (P < 0.005). Error bars represent the standard deviation.

Figure 4.

(a) Areas with more sustained activity in older adults are shown on the average structural image of all participants. Colored regions indicate areas where older adults had more sustained activity than younger adults during the category task (blue), the location task (red), or both tasks (yellow). All images entered into the conjunction analysis had P < 0.005. Activity versus baseline in the left PFC region (circled) is shown in (b), and activity for left IPL (circled) is shown in (c). Asterisks located above columns indicate that activity is significantly different from baseline (P < 0.005). Error bars represent the standard deviation.

Table 4

Greater activity in older adults compared with younger adults

Gyrus or region Hem BA x y z 
Both tasks: sustained activity      
    Inferior frontal 45 −36 29 
    Superior frontal sulcus −17 51 
    Fusiform 37 −47 −55 −14 
 19 41 −69 −6 
    Putamen  −30 −7 10 
  27 −9 
    Paracentral lobule −30 47 
    Superior occipital 19 −26 −76 33 
    Inferior parietal 40 −48 −62 33 
Category: transient activity      
    Cerebellum  −21 −39 −27 
    Putamen  28 −5 
    Cuneus 31 −66 
    Insula  −35 −22 
    Caudate nucleus  14 16 14 
  −15 17 
    Inferior parietal 40 −30 −38 48 
 40 36 −36 53 
Gyrus or region Hem BA x y z 
Both tasks: sustained activity      
    Inferior frontal 45 −36 29 
    Superior frontal sulcus −17 51 
    Fusiform 37 −47 −55 −14 
 19 41 −69 −6 
    Putamen  −30 −7 10 
  27 −9 
    Paracentral lobule −30 47 
    Superior occipital 19 −26 −76 33 
    Inferior parietal 40 −48 −62 33 
Category: transient activity      
    Cerebellum  −21 −39 −27 
    Putamen  28 −5 
    Cuneus 31 −66 
    Insula  −35 −22 
    Caudate nucleus  14 16 14 
  −15 17 
    Inferior parietal 40 −30 −38 48 
 40 36 −36 53 

Note: All clusters are ≥300 μL. Sustained maxima are the average coordinates from the regions with a group difference in sustained activity (P < 0.001) during the location and category tasks; transient maxima were taken from the t-test comparing young and old on category targets (P < 0.001). Hem = hemisphere; BA = Brodmann's area; L = left; R = right. x (right/left): negative values are in the left hemisphere; y (anterior/posterior): negative values are posterior to the zero point (located at the anterior commissure); z (superior/inferior): negative values are inferior to the plane defined by the anterior and posterior commissures.

There was no overlap between those areas showing more sustained activity in the older group and the areas where there was an age difference in transient activity. Regions with more transient activity in older adults for category targets included the caudate nucleus and putamen, medial occipital cortex, and bilateral IPL (Table 4). All of these areas also showed increased activity for category targets versus baseline in the older adults. Despite the lack of overlap, some of the areas with age differences in category target activity were similar to those with age differences in sustained activity. For example, older adults had more sustained and transient activity during the category task in different regions of the right putamen and left IPL (see Table 4). Unlike the category task, there were no regions with significant age differences in transient activity for location targets.

The difference between sustained and transient activity also was compared between young and old adults. During the category task, there were bilateral regions of auditory cortex, in Heschl's gyrus, where younger adults had more sustained activity relative to transient activity, but older adults showed similar levels of activation in both conditions (Table 5 and Fig. 5a). That is, despite the fact that both groups had reduced activity in auditory cortex when category targets were detected, this reduction was more extensive in the younger adults and included Heschl's gyrus only in the young group. In contrast, older adults had more sustained than transient activity, compared with younger adults, in the right middle frontal gyrus and left inferior PFC (Table 5). There were a number of regions where the young group had more transient activity relative to sustained activity during the category task, and the old group showed no difference. These included the middle occipital and temporal gyri, anterior cingulate, and right inferior PFC (Table 5).

Table 5

Contrasts of sustained and transient activity during category and location tasks that differ between groups

Gyrus or region Hem BA x y z Yng TvS Old TvS 
Category        
    Middle frontal 10 −39 44 20 0.09 −0.16* 
 36 31 38 0.03 −0.21* 
    Inferior frontal 47 −26 29 0.03 −0.12** 
 46 45 41 11 0.22** −0.02 
    Anterior cingulate 32 −2 26 39 0.15** −0.04 
    Superior temporal 41 −36 −22 −0.21** 0.02 
 41 41 −23 14 −0.29** 0.06 
    Middle occipital 18 34 −90 10 0.22** −0.05 
    Middle temporal 21 −55 −11 −14 0.16** −0.06 
Location        
    Medial frontal 38 42 0.24** 0.05 
    Anterior cingulate 32 11 39 15 0.16** 0.02 
    Posterior cingulate  31 −40 39 0.43** 0.17** 
    Middle occipital 18 35 −87 11 0.30** −0.02 
 19 −34 −83 0.27** 0.00 
    Fusiform 37 −46 −55 −14 0.26** −0.01 
    Inferior parietal 40 −48 −63 31 0.27** 0.00 
    Superior parietal −26 −47 50 0.17** 0.01 
Gyrus or region Hem BA x y z Yng TvS Old TvS 
Category        
    Middle frontal 10 −39 44 20 0.09 −0.16* 
 36 31 38 0.03 −0.21* 
    Inferior frontal 47 −26 29 0.03 −0.12** 
 46 45 41 11 0.22** −0.02 
    Anterior cingulate 32 −2 26 39 0.15** −0.04 
    Superior temporal 41 −36 −22 −0.21** 0.02 
 41 41 −23 14 −0.29** 0.06 
    Middle occipital 18 34 −90 10 0.22** −0.05 
    Middle temporal 21 −55 −11 −14 0.16** −0.06 
Location        
    Medial frontal 38 42 0.24** 0.05 
    Anterior cingulate 32 11 39 15 0.16** 0.02 
    Posterior cingulate  31 −40 39 0.43** 0.17** 
    Middle occipital 18 35 −87 11 0.30** −0.02 
 19 −34 −83 0.27** 0.00 
    Fusiform 37 −46 −55 −14 0.26** −0.01 
    Inferior parietal 40 −48 −63 31 0.27** 0.00 
    Superior parietal −26 −47 50 0.17** 0.01 

Note: *P < 0.005 within-group contrast for transient versus sustained, **P < 0.001 within-group contrast for transient versus sustained. All maxima had P < 0.001 for the between-group contrast and ≥300 μL. Yng TvS = percent signal change for transient minus sustained activity for younger adults. Old TvS = percent signal change for transient minus sustained activity for older adults. Hem = hemisphere; BA = Brodmann's area; L = left; R = right. x (right/left): negative values are in the left hemisphere; y (anterior/posterior): negative values are posterior to the zero point (located at the anterior commissure); z (superior/inferior): negative values are inferior to the plane defined by the anterior and posterior commissures.

Figure 5.

Differences between groups in the contrast between sustained (S) and transient (T) activity are shown on the average structural image of all participants for the category task (a) and the location task (b). Red areas showed greater transient activity, relative to sustained activity, in younger adults (and a different pattern in older adults). Blue regions had greater sustained activity, relative to transient activity, in younger adults (and a different pattern in older adults). Bar graphs show the mean percent change in sustained and transient activity (relative to baseline) for each group in the circled regions. Asterisks located above columns indicate that activity is significantly different from baseline (P < 0.005). Clusters shown are thresholded at P < 0.001 and contain at least 300 μL. Error bars represent the standard deviation.

Figure 5.

Differences between groups in the contrast between sustained (S) and transient (T) activity are shown on the average structural image of all participants for the category task (a) and the location task (b). Red areas showed greater transient activity, relative to sustained activity, in younger adults (and a different pattern in older adults). Blue regions had greater sustained activity, relative to transient activity, in younger adults (and a different pattern in older adults). Bar graphs show the mean percent change in sustained and transient activity (relative to baseline) for each group in the circled regions. Asterisks located above columns indicate that activity is significantly different from baseline (P < 0.005). Clusters shown are thresholded at P < 0.001 and contain at least 300 μL. Error bars represent the standard deviation.

During the location task, there were no significant age differences in sustained versus transient activity in auditory cortex. However, younger adults had more transient activity relative to sustained activity during the location task in a number of areas, whereas the older adults showed no significant modulation of activity in most of these regions. These areas included left IPL (in a region similar to the left IPL area with more sustained activity in older adults during both tasks), anterior cingulate gyrus, and medial PFC. More transient versus sustained activity also was seen in younger adults in the right middle occipital gyrus (Fig. 5b), an area that showed the same effect for the category task (see Table 5). One region with a somewhat different pattern was the posterior cingulate, where there was more transient than sustained activity for location in both groups, but this difference was larger in the young group (Table 5).

The differences found between younger and older adults raised the question of whether activity in any of these regions was related to performance in the older group. That is, did the degree of increased sustained activity in frontal cortex or the degree to which activity was reduced in auditory cortex to targets, have any impact on how well older adults performed on the WM tasks? To address this question, we extracted the signal (relative to baseline) in the left inferior frontal region where older adults had more activity on both tasks and in the right frontal regions where the older group had more activity for the category task. We also calculated the magnitude of signal reduction (transient minus sustained activity) in the auditory areas showing adaptation in the older group. We then assessed the correlations between these measures and performance accuracy on the category and location tasks in the older adults. Category accuracy was correlated significantly with the degree of adaptation in left auditory cortex (r = −0.46, P = 0.05) but not with adaptation in right auditory cortex or with activity in any of the frontal regions. The relation between adaptation and performance was in the expected direction, such that those older adults with larger signal decreases in left auditory cortex during the category task showed better performance (Fig. 6). Older adults' accuracy on the location task was not correlated significantly with activity in any of the frontal regions or with activity decreases in auditory cortices.

Figure 6.

This figure shows a scatter plot of accuracy on the category task in older adults and the degree to which activity in left auditory cortex is reduced for targets. Those older adults with greater reductions showed more accurate performance.

Figure 6.

This figure shows a scatter plot of accuracy on the category task in older adults and the degree to which activity in left auditory cortex is reduced for targets. Those older adults with greater reductions showed more accurate performance.

Discussion

In the current experiment, we assessed spatial and nonspatial auditory WM to determine the effects of aging on the ventral and dorsal auditory processing streams. We found that activity in these 2 streams was functionally dissociated regardless of age, as was noted earlier in the visual system (Grady et al. 1994). Both young and old groups had more activity in left anterior temporal cortex and inferior frontal gyrus during WM for sound category and more activity in right IPL and superior frontal cortex during WM for sound location. These patterns are very similar to those reported previously by our group for auditory spatial and nonspatial processing (Alain et al. 2001; Arnott et al. 2005), although more lateralized. The left-hemisphere activation seen here for the category task is likely due to the fact that we used meaningful stimuli and instructed the participants to attend to the semantic information contained in the stimuli (e.g., Cabeza and Nyberg 2000; Martin and Chao 2001; Wagner et al. 2001; Thompson-Schill 2003). Conversely, the right-hemisphere activity for sound location is in line with reports of right-hemisphere dominance for spatial attention (Corbetta et al. 1993; Nobre et al. 1997; Tanaka et al. 1999; Losier and Klein 2001). In addition, both younger and older adults had evidence of adaptation in auditory cortex during both category and location repetition, and increased activity for targets, relative to sustained activity, in medial frontal and parietal areas and in sensorimotor regions. Thus, many aspects of auditory function as reflected in these WM tasks showed no changes with age.

This is not to say, however, that no age differences were found. Older adults had more sustained activity than younger adults in left PFC, bilateral putamen, and left parietal cortex during both tasks and more transient activity during the category task in right putamen, bilateral caudate, and bilateral IPL. We attempted to eliminate age differences in WM performance by equating performance prior to scanning. In this way, we hoped to ensure that any age differences in brain activity could be interpreted without the confounding influence of performance differences. This approach was partially successful, resulting in no significant age differences in detecting location targets, but older adults had significantly lower accuracy of target detection on the category task. Given this pattern of behavioral results, it is unlikely that greater sustained activity in older adults compared with younger adults in left inferior PFC during both tasks was the result of performance differences. If increased activity in this area was solely due to less accurate performance, an age difference would not have been found for the location task. In addition, our results showed that in these WM tasks, additional PFC recruitment in older adults was a general task effect and was not limited to decisions about targets. The putative role of inferior PFC in WM maintenance (D'Esposito et al. 1999) or in attentional control of WM retrieval (Owen et al. 2005) would suggest that these tasks place a greater demand on the ability to hold auditory information “on line” in older adults. Further, the lack of a significant correlation between PFC activity and performance in the older adults indicates that this increased activity may not reflect individual differences in compensatory mechanisms, but rather age changes in task load that may support behavior generally. We also found age differences consistent with the idea that PFC activity in older adults is more bilateral than that seen in younger adults (Cabeza 2002). That is, sustained PFC activity in the right hemisphere was greater in the older adults during the category task, in which PFC activity was left sided in younger adults, and greater in left PFC during the location task, in which PFC activity was right sided in younger adults.

Some of the increased sustained activity in older adults was found in medial regions of cortex that have been described recently as part of a “default mode” network (Raichle et al. 2001; Fox et al. 2005). These default mode areas typically have reduced or suppressed activity when participants become engaged in an externally driven task. In the current experiment, this suppression of default mode activity was seen in lower sustained activity during the tasks, relative to transient activity (see Fig. 3). However, the older adults showed smaller reductions of sustained activity in some of these medial areas. This result is similar to that reported in older adults for visual tasks (Lustig et al. 2003; Grady et al. 2006) and indicates that age-related changes in default mode activity are not limited to a single sensory modality. In addition, older adults showed more sustained activity in extrastriate regions compared with younger adults, who showed reduced activity versus baseline in these areas. Reduced activity in visual cortex in young adults is consistent with earlier reports of less activity in brain regions subserving sensory modalities that are not attended (Roland 1982; Haxby et al. 1994; Amedi et al. 2005), in this case reflecting the direction of attention away from visual input and toward auditory input. Smaller reductions of activity in extrastriate cortex in older adults would suggest an altered ability to selectively allocate attention from one modality to the other, consistent with reports of age differences in selective attention both within and between modalities (e.g., Madden 1990; Allen et al. 1993; Townsend et al. 2006).

Decreased activity in auditory cortex for targets compared with sustained activity was seen in the older adults, as it was in the younger adults. However, the magnitude of this target-related reduction, or adaptation, was lower than that seen in the young adults during the category task. As this effect was seen during the task with an age difference in performance, it may be related to the underlying mechanism of the performance deficit. That is, a failure to modulate activity appropriately when a stimulus is repeated, or when a particular feature of the stimulus is repeated, could lead to reduced ability to detect this repetition. Indeed, the correlation between adaptation in left auditory cortex and accuracy on the category task in older adults supports this idea. MR adaptation in older adults has not been studied systematically, but one study assessing visual adaptation to objects found it to be equivalent in older and younger adults (Chee et al. 2006), but reduced in older adults when the task was made more complex by presenting the objects in the context of backgrounds. Our results suggest that there may be an age difference in auditory adaptation as well, similar to age reductions in habituation to auditory stimuli demonstrated electrophysiologically (Alain and Woods 1999; Fabiani et al. 2006). This result, together with the similar age difference in reduced activity of default mode regions and extrastriate cortex, suggests a failure of older adults to reduce activity where it may be appropriate or advantageous to do so. Thus, this experiment provides further evidence that age differences in deactivation may be just as important as differences in activation.

There were some brain areas where there was an age increase only for the category task, both for sustained- and target-related activity. These included right dorsolateral PFC and thalamus (sustained), as well as caudate nucleus and medial occipital cortex (transient). Activity in these areas may be related to performance, rather than age per se, as the older adults performed more poorly on the category task. In particular, right dorsolateral PFC has been implicated in manipulation and monitoring processes in WM (e.g., D'Esposito et al. 1999; Stern et al. 2000; Johnson et al. 2003), and PFC activity increases with WM task load in younger adults (Braver et al. 1997). An age-related increase in dorsolateral PFC during the category task could indicate that older adults engaged monitoring processes because they found this task more difficult. Interestingly, although there was no overlap between areas with age increases for sustained activity and those for transient activity on the category task, some of the regions were similar. This suggests that these age differences in sustained and transient brain activity reflect different mechanisms that sometimes involve similar but nonoverlapping portions of the same brain regions.

Brain areas with lower activity in older adults, relative to the younger, were mainly seen in the contrast of transient and sustained activity. There were a number of regions showing more transient activity than sustained activity in younger adults, with little modulation of activity in older adults. For both tasks, these included middle occipital regions, which may reflect some visual imagery (Amedi et al. 2005; Slotnick et al. 2005) on the part of the young adults when targets were correctly discriminated. Anterior cingulate also was more active during target detection, compared with its sustained activity, in young adults. As this area is thought to be involved in error monitoring and detection (Allman et al. 2001; Carter et al. 2001), more activity in this region may indicate that the young adults were more aware of whether or not their performance was successful.

Finally, the left IPL deserves mention, as it showed an interesting pattern of age differences. This area had greater sustained activity in older adults in both WM tasks but more transient activity in younger adults during the location task. Indeed, sustained activity in left IPL during the location task is lower than baseline activity in young adults. We have reported elsewhere that the IPL in both hemispheres is active for location and category targets in young adults (Alain et al., unpublished data), consistent with the greater transient activity seen here. Target-related activity in young adults suggests that this region participates in sensorimotor integration during these auditory tasks regardless of the specific task demands. In contrast, the older adults show greater sustained activity in left IPL, along with dorsal premotor cortex and subcortical regions linked to motor skill learning (Raz et al. 2000; Poldrack and Packard 2003), throughout the category and location blocks. This sustained activity may reflect higher tonic activity or more readiness to respond on the part of the older adults. In addition, recruitment of IPL, a dorsal stream region, for the category task in older adults is similar to the pattern of results found in the visual system, that is, overrecruitment of one stream while carrying out a task that emphasizes the other stream (Grady et al. 1994).

In conclusion, we found no age differences in the degree to which the ventral and dorsal auditory processing streams were functionally dissociated during 1-back WM tasks. Instead, the older adults showed more sustained activity in left PFC during both tasks, consistent with an age difference in the engagement of this region while maintaining auditory stimuli in WM. In addition, the older group showed less adaptation in auditory cortex, smaller task-related reductions of activity in default mode regions, and less modulation of target-related activity, relative to sustained activity, in a number of regions. These results provide further evidence that age differences in brain activity during cognitive tasks, regardless of the sensory modality, can be found in regions with task-related activations and in those with task-related deactivations. We conclude that overrecruitment of some PFC regions, particularly dorsolateral PFC, in older adults may be associated with greater task difficulty, but that not all PFC increases in older adults can be explained by lower performance. Although we did not find a significant correlation between PFC overrecruitment and performance on these tasks in the older adults, it is possible that specific patterns of activity involving PFC, as well as other brain regions, might be related to performance in older adults (e.g., Grady et al. 2005). Finally, our results are suggestive of an age-related reduction in auditory adaptation that has an impact on older adults' WM ability, indicating that further study of the effect of age on adaptation is warranted.

This work was supported by grants from the Canadian Institutes of Health Research, the Natural Sciences and Engineering Research Council of Canada, the Ontario Research Fund, and the Canadian Foundation for Innovation. CLG also is supported by the Canada Research Chairs program. The authors thank Alice Kim and the MRI technologists at Sunnybrook Health Science Centre for their assistance in carrying out this experiment. Conflict of Interest: None declared.

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