Functional topography of working memory for face or voice identity

We used functional magnetic resonance imaging (fMRI) to investigate whether the neural systems for nonspatial visual and auditory working memory exhibits a functional dissociation. The subjects performed a delayed recognition task for previously unfamiliar faces and voices and an audiovisual sensorimotor control task. During the initial sample and subsequent test stimulus presentations, activation was greater for the face than for the voice identity task bilaterally in the occipitotemporal cortex and, conversely, greater for voices than for faces bilaterally in the superior temporal sulcus/gyrus (STS/STG). Ventral prefrontal regions were activated by both memory delays in comparison with the control delays, and there was no significant difference in direct voxelwise comparisons between the tasks. However, further analyses showed that there was a subtle difference in the functional topography for two delay types within the ventral prefrontal cortex. Face delays preferentially activate the dorsal part of the ventral prefrontal cortex (BA 44/45) while voice delays preferentially activate the inferior part (BA 45/47), indicating a ventral/dorsal auditory/visual topography within the ventral prefrontal cortex. The results confirm that there is a modality-specific attentional modulation of activity in visual and auditory sensory areas during stimulus presentation. Moreover, within the nonspatial information-type domain, there is a subtle across-modality dissociation within the ventral prefrontal cortex during working memory maintenance of faces and voices.

Introduction

Studies on working memory have suggested that there are dissociable domain-dependent functional topographies within the prefrontal cortex for working memory processing of verbal, spatial, and nonspatial visual information (for reviews, see Courtney et al., 1998b, Levy and Goldman-Rakic, 2000, Smith and Jonides, 1999). Dorsal prefrontal regions including the superior frontal sulcus have been proposed to be specialized for working memory maintenance of visual locations (e.g., Courtney et al., 1996, Courtney et al., 1998a, Glahn et al., 2003, Gruber and von Cramon, 2003, Munk et al., 2002, Sala et al., 2003), whereas ventral prefrontal regions are more active for maintenance of nonspatial visual and verbal information (e.g., Awh et al., 1996, Courtney et al., 1997, Courtney et al., 1998a, Jonides et al., 1997, Nystrom et al., 2000, Rämä et al., 2001). It has been proposed that the auditory system is also organized into two domain-dependent, spatial and nonspatial, processing streams, similar to that seen in the visual system (Ungerleider and Haxby, 1994, Ungerleider and Mishkin, 1982). Different regions of the auditory cortex have been shown to be differentially responsive to spatial and spectral features of auditory stimulation and these regions in the auditory belt cortex have been shown to project to distinct regions of the temporal, parietal, and prefrontal cortices (Romanski et al., 1999, Tian et al., 2001; for review, see Rauschecker and Tian, 2000). Recently, we and others have shown that during auditory working memory, maintenance of spatial and nonspatial information modulates activity preferentially in dorsal and ventral auditory pathways, respectively (Alain et al., 2001, Arnott et al., 2002, Rämä et al., 2004), suggesting that dorsal/ventral, spatial/nonspatial functional topography of the frontal cortex is similar for auditory and visual working memory. However, without a direct comparison to a comparable visual task in the same group of subjects, we cannot determine whether these auditory activations are in exactly the same anatomical location as the analogous visual working memory regions.

Single neurons showing selective responses during perceptual processing of monkey vocalizations have been localized within the ventral prefrontal cortex, but locations of auditory neurons were found to be more anterior and lateral than those of visually responsive neurons, suggesting that auditory and visual working memory systems are dissociable within the ventral prefrontal cortex (Romanski and Goldman-Rakic, 2002). It appears, however, that only small regions in the prefrontal cortex are modality-specific for auditory and visual information (Poremba et al., 2003).

In the present study, we aimed to compare the neural systems involved in working memory for face and voice identities. We used voices because prefrontal neurons in monkeys were shown to respond better to natural sounds or monkey vocalizations than to pure tones (Azuma and Suzuki, 1984, Romanski and Goldman-Rakic, 2002), and also because the anterior part of the superior temporal sulcus (STS) in humans has been shown to exhibit selective activation for voices, leading to the suggestion that this region may be analogous to the face-sensitive area in the fusiform gyrus, which is a part of the ventral visual pathway (Belin et al., 2000, Belin et al., 2002, Shah et al., 2001). The subjects performed a delayed recognition task for previously unfamiliar faces and voices. To emphasize attentional and working memory processes, rather then perceptual mechanisms that are known to be different for auditory and visual stimuli, the faces and voices were presented simultaneously and the subjects were instructed to keep in mind either the face or the voice. Voice samples were non-imageable two-word phrases (e.g., “further consideration”) and were obtained by asking several individuals to utter a single word with a neutral emotional intonation. To find out whether a functional dissociation between auditory and visual information might occur during specific phases of this working memory task, we performed separate analyses of task-related activations evoked during the sample, delay, and test periods of the two memory tasks. The aim of the study was to find out (1) whether the neural mechanisms underlying encoding, maintenance, and recognition of faces and voices in working memory are dissociated or (2) whether nonspatial working memory activates common neuronal structures independent of stimulus modality. It was hypothesized that while neural structures in posterior cortical areas are segregated for modality-specific processing of identity information (face vs. voice), the ventral prefrontal cortex would be activated similarly for both working memory for faces and for voices. Such a result would suggest that a common neural network in the prefrontal cortex handles nonspatial information independent of the stimulus modality.