Neuronal Assemblies Evidence Distributed Interactions within a Tactile Discrimination Task in Rats

Abstract

Accumulating evidence suggests that neural interactions are distributed and relate to animal behavior, but many open questions remain. The neural assembly hypothesis, formulated by Hebb, states that synchronously active single neurons may transiently organize into functional neural circuits—neuronal assemblies (NAs)—and that would constitute the fundamental unit of information processing in the brain. However, the formation, vanishing, and temporal evolution of NAs are not fully understood. In particular, characterizing NAs in multiple brain regions over the course of behavioral tasks is relevant to assess the highly distributed nature of brain processing. In the context of NA characterization, active tactile discrimination tasks with rats are elucidative because they engage several cortical areas in the processing of information that are otherwise masked in passive or anesthetized scenarios. In this work, we investigate the dynamic formation of NAs within and among four different cortical regions in long-range fronto-parieto-occipital networks (primary somatosensory, primary visual, prefrontal, and posterior parietal cortices), simultaneously recorded from seven rats engaged in an active tactile discrimination task. Our results first confirm that task-related neuronal firing rate dynamics in all four regions is significantly modulated. Notably, a support vector machine decoder reveals that neural populations contain more information about the tactile stimulus than the majority of single neurons alone. Then, over the course of the task, we identify the emergence and vanishing of NAs whose participating neurons are shown to contain more information about animal behavior than randomly chosen neurons. Taken together, our results further support the role of multiple and distributed neurons as the functional unit of information processing in the brain (NA hypothesis) and their link to active animal behavior.

Frequency-specific coupling in fronto-parieto-occipital cortical circuits underlie active tactile discrimination

“…These data are consistent with results shown by other authors who utilized the same task in S1 5 , 6 , 40 and V1 45 . We also found extensive neuronal firing rate modulations in the ACC and PPC, which demonstrate the clear involvement of these cortical areas in tactile discrimination according to electrophysiological 35 , 46 , 47 and functional imaging studies 48 , 49 . The presence of marked modulations in the neuronal firing rate in all task phases (anticipation, discrimination, response and reward) also suggest that even such a simple tactile discrimination task requires the involvement of vast cortical circuits to be performed properly.…”

Distributed cell assemblies spanning prefrontal cortex and striatum

“…Conversely, there is little evidence for co-activation at such a fast ($10 ms) timescale or for distributed synchrony, i.e., multi-neuronal assemblies spanning multiple cortical areas (e.g., for sensorimotor processing). 12,13 One system to study distributed synchrony in cortical-subcortical areas is the cortico-striatal pathway, which is composed of multiple parallel loops for sensorimotor, associative, and limbic processing. The latter includes monosynaptic projections from rat medial prefrontal cortex (PFC) to ventral and medial striatum (STR), which projects polysynaptically back to PFC.…”

Motor execution, but not learning, improves upon increased layer 5 specific Martinotti cell excitation

“…We found an increased LFP amplitude under CLZ treatment in Chrna2-Cre+ mice compared to control mice during successful (p=1.8e-02, Figure 6C, left), as well as failed prehensions (p=4.8e-02, Figure 6C Hebbian learning postulates that when neurons fire synchronously, they reinforce synaptic efficiency and form an assembly. The original theory has been extended to include all cells with above-chance interactions, leading to variable definitions of neural assemblies [92]. We here adhere to the proposition that assemblies are formed by neurons that together increase their average firing rates for a specific period [93,40], and that they can harbor varying degrees of temporal precision, scale and internal structure [94].…”

“…In the naive session, we identified a total of 23 assem- trol mice (saline session 3: n=6, prehensions=974, success ratio=13.48%; CLZ session 3: n=6, prehensions=858, success ratio=14.82%; t-test eff. size = 0.009, p=0.987; to variable definitions of neural assemblies [90]. We here 1271 adhere to the proposition that assemblies are formed by 1272 neurons that together increase their average firing rates for 1273 a specific period [91,74], and that they can harbor varying 1274 degrees of temporal precision, scale and internal structure 1275 [92].…”