The Behavioral Relevance of Cortical Neural Ensemble Responses Emerges Suddenly

Abstract

Whereas many laboratory-studied decisions involve a highly trained animal identifying an ambiguous stimulus, many naturalistic decisions do not. Consumption decisions, for instance, involve determining whether to eject or consume an already identified stimulus in the mouth and are decisions that can be made without training. By standard analyses, rodent cortical single-neuron taste responses come to predict such consumption decisions across the 500 ms preceding the consumption or rejection itself; decision-related firing emerges well after stimulus identification. Analyzing single-trial ensemble activity using hidden Markov models, we show these decision-related cortical responses to be part of a reliable sequence of states (each defined by the firing rates within the ensemble) separated by brief state-to-state transitions, the latencies of which vary widely between trials. When we aligned data to the onset of the (late-appearing) state that dominates during the time period in which single-neuron firing is correlated to taste palatability, the apparent ramp in stimulusaligned choice-related firing was shown to be a much more precipitous coherent jump. This jump in choice-related firing resembled a step function more than it did the output of a standard (ramping) decision-making model, and provided a robust prediction of decision latency in single trials. Together, these results demonstrate that activity related to naturalistic consumption decisions emerges nearly instantaneously in cortical ensembles.

Itinerancy between attractor states in neural systems

“…Hidden Markov models of multiple simultaneously recorded in vivo spike trains have revealed transitions between relatively stable discrete activity states in premotor and prefrontal cortex of monkey performing a spatial short-term memory task [17,25,26] or freely viewing a scene [27], and in gustatory cortex of rats processing tastants [28]. The timing of such state transitions both correlates with ongoing behavior [27,29] and is predictive of an ensuing response [30]. …”

“…Evidence for a delayed rapid transition from one discrete attractor state to another during decision making has been accrued during taste processing (where the decision is to expel or ingest a tastant) [28,30], in a somatosensory task [80], and in a detection of motion direction task [32]. However, an alternative analysis of the latter task revealed ramping as the typical dynamics during stimulus acquisition, with rapid transitions corresponding only to changes of mind [81].…”

Single and population coding of taste in the gustatory-cortex of awake mice

“…In contrast, a good deal of coherent progress has been made toward characterizing primary gustatory cortical (GC) taste responses in awake rats, mainly (but not ubiquitously) using electrophysiology. This work has exposed reliable properties of taste spiking activity in relation to behavior, specifically revealing: 1) that single-neuron taste responses vary widely in breadth, with responses to multiple tastes appearing in the same region, and even within the same single neurons (Katz et al, 2001;Fontanini & Katz, 2006;Accolla et al, 2007;Samuelsen et al, 2013); 2) that these responses progress through a series of firing-rate "epochs," coding in turn the presence, physical properties, and palatability of a taste across 1-1.5s (Katz et al, 2001;Bahar et al, 2004;Sadacca et al, 2012;Maier & Katz, 2013;Samuelsen et al, 2013); 3) that the late-epoch palatabilityrelated firing is uniquely affected by experience-driven shifts of taste palatability (Bahar et al, 2004;Fontanini & Katz, 2006;Grossman et al, 2008;Moran and Katz., 2014); and 4) that in single trials the onset of palatability is a sudden, coherent network phenomenon, the timing of which predicts and impacts behavior (Jones et al, 2007;Sadacca et al, 2016;Li et al, 2016). A test of whether mouse GC neurons respond in a like manner has not yet been performed.…”

A gustocentric perspective to understanding primary sensory cortices

“…The description of sudden transitions between states lead to the suggestion that a stochastic, jumping model of decision making could account for ingestive decisions more accurately than the traditional diffusion-to-bound model, particularly in conditions of noisy signals [29,30] (Figure 1). Recent data confirmed this suggestion in both GC [31] and lateral intraparietal area (LIP) [32]. Finally, recent work unveiled that metastability is not limited to evoked activity, but can also be observed during spontaneously ongoing activity [28] (Figure 1d).…”

“…Specifically, it has been demonstrated that valence coding emerges with a slow latency (i.e., ~ 1 second) compared to stimulus onset. Population analyses with HMM confirmed this observation and provided further evidence indicating that, at a single trial level, valence coding emerges as a sudden and rapid change in the state of ensemble activity [31]. Recent ensemble recordings in rat GC showed that gapes (i.e.…”