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Willett, S. M.

Publications and source records attributed to Willett, S. M..

5 recordsLinked to original sources

Neural multiplexing vs place coding: Multiplexing steps in when most needed

Sensory scenes contain many different stimuli. Two complementary theories about how the brain segregates signals from different stimuli concern (a) time division multiplexing, such that neurons switch between encoding each item over time; and/or (b) place coding, such that different populations of neurons encode each item. Such time division multiplexing would appear to be required when the population of neurons responsive to each stimulus overlaps, as place coding lacks the granularity to resolve the two stimuli. This predicts that as responses to component stimuli become more similar, and thus less well resolved by place coding, there would be a greater incidence of multiplexing. We tested this hypothesis using single-unit responses in the macaque inferior colliculus to combinations of two sounds of varying center frequencies (given that sound frequency is place coded in this structure). We found that neurons were more likely to multiplex when their responses to each individual sound was more similar, differentiating signals whose neural representations would otherwise be less distinct. This finding supports the theory that neurons multiplex to maintain information about concurrent stimuli when place coding is insufficient to prevent largely overlapping responses in the neural population.

neuroscience↗

Multiple objects evoke fluctuating responses in several regions of the visual pathway

How neural representations preserve information about multiple stimuli is mysterious. Because tuning of individual neurons is coarse (for example, visual receptive field diameters can exceed perceptual resolution), the populations of neurons potentially responsive to each individual stimulus can overlap, raising the question of how information about each item might be segregated and preserved in the population. We recently reported evidence for a potential solution to this problem: when two stimuli were present, some neurons in the macaque visual cortical areas V1 and V4 exhibited fluctuating firing patterns, as if they responded to only one individual stimulus at a time (Jun et al., 2022). However, whether such an information encoding strategy is ubiquitous in the visual pathway and thus could constitute a general phenomenon remains unknown. Here we provide new evidence that such fluctuating activity is also evoked by multiple stimuli in visual areas responsible for processing visual motion (middle temporal visual area, MT), and faces (middle fundus and anterolateral face patches in inferotemporal cortex - areas MF and AL), thus extending the scope of circumstances in which fluctuating activity is observed. Furthermore, consistent with our previous results in the early visual area V1, MT exhibits fluctuations between the representations of two stimuli when these form distinguishable objects but not when they fuse into one perceived object, suggesting that fluctuating activity patterns may underlie visual object formation. Taken together, these findings point toward an updated model of how the brain preserves sensory information about multiple stimuli for subsequent processing and behavioral action. Impact StatementNeural fluctuations in multiple areas along the visual cortical hierarchy could allow the brain to represent distinct co-occurring visual stimuli.

neuroscience↗

Microsaccades are directed towards the midpoint between targets in a variably cued attention task

Reliable, non-invasive biomarkers that reveal the internal state of a subject are an invaluable tool for neurological diagnoses. Small fixational eye movements, called microsaccades, are a candidate biomarker thought to reflect a subjects focus of attention (1, 2). The linkage between the direction of microsaccades and attention has mainly been demonstrated using explicit and unambiguous attentional cues. However, the natural world is seldom predictable and rarely provides unambiguous information. Thus, a useful biomarker must be robust to such changes in environmental statistics. To determine how well microsaccades reveal visual-spatial attention across behavioral contexts, we analyzed these fixational eye movements in monkeys performing a conventional change detection task. The task included two stimulus locations and variable cue validities across blocks of trials. Subjects were adept at the task, showing precise and graded modulations of visual attention for subtle target changes and performing better and faster when the cue was more reliable (3). However, over tens of thousands of microsaccades, we found no difference in microsaccade direction between cued locations when cue variability was high nor between hit and miss trials. Instead, microsaccades were made towards the midpoint of the two target locations, not towards individual targets. Our results suggest that the direction of microsaccades should be interpreted with caution and may not be a reliable measure of covert spatial attention in more complex viewing conditions. Significance StatementSmall fixational eye movements called microsaccades are thought to "point" towards a location that is being attended in the visual periphery. This phenomenon has largely been studied using visual cues that unambiguously indicate the location of the upcoming stimulus change. Because the natural world is rarely unambiguous, we studied the relationship between microsaccade direction and spatial attention using less reliable cues. We found that monkeys microsaccade directions in a standard visuospatial attention task did not indicate the animals focus of attention, despite behavioral and neuronal evidence of spatial attention. Instead, microsaccades were made towards the midpoint between the target locations in both animals, suggesting a more complex relationship between microsaccades and attention in naturalistic settings.

animal behavior and cognition↗

Multiple sounds induce frequency tuning modulations that degrade stimulus information in monkey inferior colliculus

How we distinguish multiple simultaneous stimuli is uncertain, particularly given that such stimuli sometimes recruit largely overlapping populations of neurons. One commonly proposed hypothesis is that the sharpness of tuning curves might change to limit the number of stimuli driving any given neuron when multiple stimuli are present. To test this hypothesis, we recorded the activity of neurons in the inferior colliculus while monkeys made saccades to either one or two simultaneous sounds differing in frequency and spatial location. Although monkeys easily distinguished simultaneous sounds ([~]90% correct performance), the frequency selectivity of inferior colliculus neurons on dual sound trials did not improve in any obvious way. Frequency selectivity was degraded on dual sound trials compared to single sound trials: neural response functions broadened, and frequency accounted for less of the variance in firing rate. These changes in neural firing led a maximum-likelihood decoder to perform worse on dual sound trials than on single sound trials. These results fail to support the hypothesis that changes in frequency response functions serve to reduce the overlap in the representation of simultaneous sounds. Instead, these results suggest that alternative possibilities, such as recent evidence of alternations in firing rate between the rates corresponding to each of the two stimuli, offer a more promising approach. Graphic AbstractHow sensory representations encode multiple stimuli despite coarse coding is unknown. Using a maximum likelihood decoder operating on the spike count response patterns of monkey inferior colliculus neurons, we show a marked reduction in decoding accuracy when two sounds are presented compared to one. The decoding was inferior to the behavioral performance of the animals, and thus suggests the presence of alternative coding strategies. O_FIG O_LINKSMALLFIG WIDTH=184 HEIGHT=200 SRC="FIGDIR/small/187021v5_ufig1.gif" ALT="Figure 1"> View larger version (17K): org.highwire.dtl.DTLVardef@e028e3org.highwire.dtl.DTLVardef@9c7475org.highwire.dtl.DTLVardef@1a1e922org.highwire.dtl.DTLVardef@d0ddf8_HPS_FORMAT_FIGEXP M_FIG C_FIG

neuroscience↗

Evidence for time division multiplexing of multiple simultaneous itemsin a sensory coding bottleneck

How the brain preserves information about multiple simultaneous items is poorly understood. We report that single neurons can represent multiple different stimuli by interleaving different signals across time. We record single units in an auditory region, the inferior colliculus, while monkeys localize 1 or 2 simultaneous sounds. During dual-sound trials, we find that some neurons fluctuate between firing rates observed for each single sound, either on a whole-trial or on a sub-trial timescale. These fluctuations are correlated in pairs of neurons, can be predicted by the state of local field potentials prior to sound onset, and, in one monkey, can predict which sound will be reported first. We find corroborating evidence of fluctuating activity patterns in a separate data set involving responses of inferotemporal cortex neurons to multiple visual stimuli. Alternation between activity patterns corresponding to each of multiple items may therefore be a general strategy to enhance the brain processing capacity, potentially linking such disparate phenomena as variable neural firing, neural oscillations, and limits in attentional/memory capacity.

neuroscience↗