Category-selective phase coding in the superior temporal sulcus

Abstract

Object perception and categorization can occur so rapidly that behavioral responses precede or co-occur with the firing rate changes in the object-selective neocortex. Phase coding could, in principle, support rapid representation of object categories, whereby the first spikes evoked by a stimulus would appear at different phases of an oscillation, depending on the object category. To determine whether object-selective regions of the neo-cortex demonstrate phase coding, we presented images of faces and objects to two monkeys while recording local field potentials (LFP) and single unit activity from object-selective regions in the upper bank superior temporal sulcus. Single units showed preferred phases of firing that depended on stimulus category, emerging with the initiation of spiking responses after stimulus onset. Differences in phase of firing were seen below 20 Hz and in the gamma and high-gamma frequency ranges. For all but the <20-Hz cluster, phase differences remained category-specific even when controlling for stimulus-locked activity, revealing that phase-specific firing is not a simple consequence of category-specific differences in the evoked responses of the LFP. In addition, we tested for firing rate-to-phase conversion. Category-specific differences in firing rates accounted for 30-40% of the explained variance in phase occurring at lower frequencies (<20 Hz) during the initial response, but was limited (<20% of the explained variance) in the 30-to 60-Hz frequency range, suggesting that gamma phase-of-firing effects reflect more than evoked LFP and firing rate responses. The present results are consistent with theoretical models of rapid object processing and extend previous observations of phase coding to include object-selective neocortex.category coding | primate | visual perception A rtificial systems have yet to replicate the speed and accuracy of our ability to categorize objects. One challenge has been to understand how the visual system accomplishes such a task, when the speed of recognition (<200 ms) is estimated to accommodate approximately one spike per neuron in a feed-forward "sweep" through the visual system (1-4). Prima facie, such a fast reaction time seems incompatible with the typical ratecoding scheme used to describe neural discrimination of object categories. Given these considerations, the fastest and smallest temporal window for decoding in face/object-selective cells in inferior temporal cortex (IT) would be ∼100-150 ms after stimulus onset. In contrast, rate-based decoding is typically based on windows of 50-500 ms (5, 6), positioned 100 ms after stimulus onset (7,8). Considering that downstream movement planning is still needed, this suggests that some categorization behaviors are occurring during the neural responses thought to underlie them. As a consequence of this temporal bottleneck, several alternative schemes have emerged to accommodate rapid coding in face-and object-selective cells.One of these alternative schemes is phase coding, or phase-offiring coding, invol...

Phase of Firing Coding of Learning Variables across Prefrontal Cortex, Anterior Cingulate Cortex and Striatum during Feature Learning

“…By finding evidence for such a temporal multiplexing in the beta frequency band we critically extend previous reports of phase encoding of information for object features, object identities, and object categories at theta, alpha and gamma frequencies (Kayser et al, 2012;Siegel et al, 2009;Turesson et al, 2012;Womelsdorf et al, 2012). In our study, the beta rhythmic phaseof-firing multiplexing applied to complex learning variables that were needed to succeed in the behavioral learning task.…”

Oscillatory dynamics of perceptual to conceptual transformations in the ventral visual pathway

“…Previous studies in both humans and nonhuman primates have identified category-specific phase coding of objects, where different object categories have different preferred phases associated with neural activity (Turesson et al, 2012;Watrous et al, 2015b). Here, we go beyond phase dissociations between different categories, by showing that the variability in phase information relates to variability in the stimulus properties, and is the case for both visual and semantic properties.…”

“…Oscillations are a ubiquitous property of the brain, and are known to be modulated by various aspects of vision and memory in humans (Fell and Axmacher, 2011;Hanslmayr et al, 2012;Helfrich and Knight, 2016;Jensen et al, 2014;Watrous et al, 2015a). Recent studies have begun to show how the ongoing phase of an oscillation can be used to decode specific stimuli (Lopour et al, 2013;Ng et al, 2013;Schyns et al, 2011;Turesson et al, 2012;Watrous et al, 2015b). These studies have shown that frequency-specific activity can be used to decode the specific features of visual objects, or object categories, suggesting that oscillatory phase could provide a mechanism for encoding stimulus information within a region.…”

Hippocampal gamma‐band Synchrony and pupillary responses index memory during visual search

“…The gamma‐band phase with the strongest unit activity could vary across condition (Senior et al, ; Colgin et al, ; Turesson et al, ; Womelsdorf et al, ) independent of the strength of locking. Thus, in addition to the spike‐field coherence, we extracted the instantaneous phase from the 50–70 Hz band using the Hilbert transform to see if the peak MUA responses occurred at different phases of gamma as a function of scene repetition.…”