Stimulus-Specific Delay Activity in Human Primary Visual Cortex

Abstract

Working memory (WM) involves maintaining information in an on-line state. One emerging view is that information in WM is maintained via sensory recruitment, such that information is stored via sustained activity in the sensory areas that encode the to-be-remembered information. Using functional magnetic resonance imaging, we observed that key sensory regions such as primary visual cortex (V1) showed little evidence of sustained increases in mean activation during a WM delay period, though such amplitude increases have typically been used to determine whether a region is involved in on-line maintenance. However, a multivoxel pattern analysis of delay-period activity revealed a sustained pattern of activation in V1 that represented only the intentionally stored feature of a multifeature object. Moreover, the pattern of delay activity was qualitatively similar to that observed during the discrimination of sensory stimuli, suggesting that WM representations in V1 are reasonable "copies" of those evoked during pure sensory processing.Working memory (WM) allows the on-line storage of behaviorally relevant information. One emerging view is that WM is supported by the same neural mechanisms that encode the sensory information being remembered (we term this the sensory-recruitment model of WM; see Awh & Jonides, 2001;D'Esposito, 2007;Jonides, Lacey, & Nee, 2005;Postle, 2006). For example, neurons in face-selective regions of inferotemporal cortex show sustained amplitude increases while an observer is holding a face in WM (Chelazzi, Miller, Duncan, & Desimone, 1993;Courtney, Ungerleider, Keil, & Haxby, 1997;Druzgal & D'Esposito, 2001;Lepsien & Nobre, 2007;Miller, Li, & Desimone, 1993;Ranganath, Cohen, Dam, & D'Esposito, 2004). The sensory-recruitment hypothesis assumes that this activity represents the specific stimulus values of the stored items. Here we report a study in which functional magnetic resonance imaging (fMRI) and multivoxel pattern analysis (MVPA) provided direct support for this claim, showing that activation patterns in relevant sensory regions represent the specific stimulus value that is held in WM.MVPA provides a useful tool for identifying the neural regions that mediate WM by focusing on changes in activation patterns as opposed to simply changes in the mean amplitude of the blood-oxygenation-level-dependent (BOLD) response. For example, Offen, Schluppeck, and Heeger (in press) used fMRI to index activation changes in primary visual cortex (V1), a region known to represent orientation and spatial frequency. Although mean response amplitudes in V1 increased during sustained deployments of spatial attention, activation levels were indistinguishable from a low-level baseline when information about orientation (or spatial frequency) was stored in WM. This finding appears to contradict the sensory-recruitment model. preferentially to the remembered orientation should become more active, whereas neurons tuned away from the remembered orientation should be suppressed (relatively speaking; see, e.g.,...

Laminar fMRI: Applications for cognitive neuroscience

“…Similarly, mental imagery might involve the recruitment of early visual cortex as a 'cognitive blackboard', with higher areas inducing virtual sensory data in V1 to represent an imagined stimulus (Roelfsema & De Lange, 2016). These hypotheses are supported by brain decoding studies, which show that patterns of activity across early visual cortex during the maintenance of a previously presented grating stimulus (Harrison & Tong, 2009;Serences et al, 2009) or an internally imagined one (Albers et al, 2013) are similar to patterns induced by bottom-up perception of the same stimulus. Moreover, in the study by (Albers et al, 2013) a decoder trained on patterns induced during memory was equally accurate in decoding the orientation of an imagined grating as a classifier trained on patterns induced by perception, implying that representations of memory and imagery may be formed by the same perceptual mechanisms (Tong, 2013).…”

Visual working memory buffers information retrieved from visual long-term memory

“…Specifically, we show that alpha-band oscillations can be used to track when a memory representation changes its state from a passive long-term memory to an active working memory (44). Given the evidence that the similar patterns of neural activity represent perceptual inputs and maintain those representations in working memory (45)(46)(47), we propose that the alpha-band activity we measured indicates a shift to the same active state by the neurons that store longterm memories.…”

The relationship between visual working memory and attention: retention of precise colour information in the absence of effects on perceptual selection

“…A second possibility is that the two forms of representation differ in the extent to which they involve sustained activation of featurespecific neural populations in visual-sensory regions. Several studies have indicated that delay-period activity in V1 through inferotemporal cortex is correlated with VWM content [29][30][31], and VWM content interacts with the initial sensory processing of visual stimuli, increasing the salience of memorymatching objects and biasing attention towards them [4]. Items in VWM that do not interact with perceptual selection would not be accompanied by visual-sensory activation during maintenance, would not interact with the sensory processing of new stimuli, and thus would not bias perceptual selection.…”