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What are the spatial and temporal scales of brainwide neuronal activity, and how do activities at different scales interact? We used SCAPE microscopy to image a large fraction of the central brain of adult Drosophila melanogaster with high spatiotemporal resolution while flies engaged in a variety of behaviors, including running, grooming and flailing. This revealed neural representations of behavior on multiple spatial and temporal scales. The activity of most neurons across the brain correlated (or, in some cases, anticorrelated) with running and flailing over timescales that ranged from seconds to almost a minute. Grooming elicited a much weaker global response. Although these behaviors accounted for a large fraction of neural activity, residual activity not directly correlated with behavior was high dimensional. Many dimensions of the residual activity reflect the activity of small clusters of spatially organized neurons that may correspond to genetically defined cell types. These clusters participate in the global dynamics, indicating that neural activity reflects a combination of local and broadly distributed components. This suggests that microcircuits with highly specified functions are provided with knowledge of the larger context in which they operate, conferring a useful balance of specificity and flexibility.

Neurons in piriform cortex receive input from a random collection of glomeruli, resulting in odor representations that lack the stereotypic organization of the olfactory bulb. We have performed in vivo optical imaging and mathematical modeling to demonstrate that correlations are retained in the transformation from bulb to piriform cortex, a feature essential for generalization across odors. Random connectivity also implies that the piriform representation of a given odor will differ among different individuals and across brain hemispheres in a single individual. We show that these different representations can nevertheless support consistent agreement about odor quality across a range of odors. Our model also demonstrates that, whereas odor discrimination and categorization require far fewer neurons than reside in piriform cortex, consistent generalization may require the full complement of piriform neurons.

SummaryIn what regime does the cortical circuit operate? Our intracellular studies of surround suppression in cat primary visual cortex (V1) provide strong evidence on this question. Although suppression has been thought to arise from an increase in lateral inhibition, we find that the inhibition that cells receive is reduced, not increased, by a surround stimulus. Instead, suppression is mediated by a withdrawal of excitation. Thalamic recordings and previous work show that these effects cannot be explained by a withdrawal of thalamic input. We find in theoretical work that this behavior can only arise if V1 operates as an inhibition-stabilized network (ISN), in which excitatory recurrence alone is strong enough to destabilize visual responses but feedback inhibition maintains stability. We confirm two strong tests of this scenario experimentally and show through simulation that observed cell-to-cell variability in surround effects, from facilitation to suppression, can arise naturally from variability in the ISN.