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.

Keywords: distributed cortical interactions; independent component analysis; neuronal assemblies; rat; tactile discrimination.

Figure 1

(A) Schematics of the behavioral apparatus: the animal has to discriminate between a wide or narrow aperture employing only their mystacial vibrissae in order to get a water reward (adapted from Krupa et al., 2001). (B) Distribution of reaction times considering 764 trials from all 7 rats: time to reach the Nose Poke (NP) or Reward (RW) sites with respect to the Central Door event (t = 0 s). (C) Reaction times per animal (mean ± std).

Figure 2

Schematics of NA detection: Spikes are recorded from a pool of cortical cells (A), forming a set of spike trains (B). The trains are binned and fed into an assembly detection algorithm (C). A relation matrix is built based on the covariance of spike trains, followed by a PCA+ICA community detection algorithm. The assembly detection algorithm identifies neurons with joint activations (pink and orange) and independent neurons (blue) (D). In this work, functional NAs are defined by time-specific coherent modulations in the firing rate. Notice that one neuron may participate in more than one NA.

Figure 3

Peri-stimulus time histograms of neuronal responses of single cells. Panels show 3 representative neurons from diverse subjects in each of the brain regions recorded. Neuronal data was binned using a sliding 10 ms time-window (no overlap). The baseline neural activity is defined as the [−3 −2] s period. Red (blue) horizontal lines indicate significant increase (decrease) in firing modulations; purple (yellow) lines relate to the baseline (analyzed) period; dashed horizontal lines depict the MFR in the whole period. Time t = 0 mark the moment rats reach the NP (dashed green horizontal line). Blue points indicate the beginning of trials (Central Door) and red points indicate the water reward delivery.

Figure 4

Multiphasic neurons mean firing rate (bin = 50 ms, no overlap, z-scored) of all animals in each of the four recorded cortical areas. Red (black) lines depict the activity when reward was at the left (right) hand side. Time t = 0 s marks the moment rats reach the NP. Shaded regions relate to the standard error of the mean (calculated across the total number of recorded cells, described in Table 2). Curves are smoothed with a 10-point moving average filter. Dashed blue (red) vertical lines indicate the approximate beginning of trials (reward) time.

Figure 5

(A) Mean animal response predicted with a SVM decoder. The decoder is fed either with the activity from all recorded cells within each cortical region (black), or with the activity from each neuron, individually. Average (best) single-neuron decoding accuracy is shown in blue (red). For each trial, the decoder mapped seven consecutive 50 ms windows of spike activity (50 ms time step) into left or right reward side. Labeled time points indicate the ending of the sliding time windows. Curves are smoothed using a 5-point moving average filter. Time t = 0 s marks the moment rats reach the NP. Shaded regions relate to the standard error of the mean (calculated across the total number of animals). Dashed blue (red) vertical lines indicate the approximate beginning of trials (reward) time. (B) Mean ± std of animal response predicted with a SVM decoder using the neural activity from a 350 ms window immediately prior to or after the central door (CD), nose-poke (NP), and reward (RW) events.

Figure 6

(A) NAs found for Rat 1. For each trial, 3 s data segments were selected centered on NP. Each small circle corresponds to one recorded neuron (see Table 2); lines of equal color connect neurons that belong to the same NA. (B) NA summary for all animals. Lines connect cortical areas where at least 10% of cells were engaged in the same (color-coded) NA. The thicker the connections, the greater the number of animals presenting NAs between the indicated cortical regions. For example, in the NP time window, 3 animals presented functional interactions within PFC, S1 and V1 (blue NA); before NP, only one animal displayed this interaction. Brain template adapted from Töle (2014).

Figure 7

Decoding accuracy of NAs and random neurons. In black, we show the decoding accuracy using solely neurons from the NAs identified with ICA; in blue, the same cells were used but labels of animal response (left/right) are shuffled. In red, we use a random group of neurons out of the total population, containing the same number of cells as the identified NAs. We recall that no further restriction is imposed, i.e., the selection of cells belonging to other NAs, which also significantly modulate their firing rate, is possible. The shuffling process was repeated 100 times. In green, we depict the moments in which the decoding accuracy in NA and random cells are significantly different (p < 0.05). Time t = 0 s marks the moment rats reach the NP. Dashed blue (red) vertical lines indicate the approximate beginning of trials (reward) time.