Coordinated population activity underlying texture discrimination in rat barrel cortex

Rodents can robustly distinguish fine differences in texture using their whiskers, a capacity that depends on neuronal activity in primary somatosensory \u201cbarrel\u201d cortex. Here we explore how texture was collectively encoded by populations of three to seven neuronal clusters simultaneously recorded from barrel cortex while a rat performed a discrimination task. Each cluster corresponded to the single-unit or multiunit activity recorded at an individual electrode. To learn how the firing of different clusters combines to represent texture, we computed population activity vectors across moving time windows and extracted the signal available in the optimal linear combination of clusters. We quantified this signal using receiver operating characteristic analysis and compared it to that available in single clusters. Texture encoding was heterogeneous across neuronal clusters, and only a minority of clusters carried signals strong enough to support stimulus discrimination on their own. However, jointly recorded groups of clusters were always able to support texture discrimination at a statistically significant level, even in sessions where no individual cluster represented the stimulus. The discriminative capacity of neuronal activity was degraded when error trials were included in the data, compared to only correct trials, suggesting a link between the neuronal activity and the animal's performance. These analyses indicate that small groups of barrel cortex neurons can robustly represent texture identity through synergistic interactions, and suggest that neurons downstream to barrel cortex could extract texture identity on single trials through simple linear combination of barrel cortex responses

Neuronal Activity in Rat Barrel Cortex Underlying Texture Discrimination

Rats and mice palpate objects with their whiskers to generate tactile sensations. This form of active sensing endows the animals with the capacity for fast and accurate texture discrimination. The present work is aimed at understanding the nature of the underlying cortical signals. We recorded neuronal activity from barrel cortex while rats used their whiskers to discriminate between rough and smooth textures. On whisker contact with either texture, firing rate increased by a factor of two to ten. Average firing rate was significantly higher for rough than for smooth textures, and we therefore propose firing rate as the fundamental coding mechanism. The rat, however, cannot take an average across trials, but must make an immediate decision using the signals generated on each trial. To estimate single-trial signals, we calculated the mutual information between stimulus and firing rate in the time window leading to the rat's observed choice. Activity during the last 75 ms before choice transmitted the most informative signal; in this window, neuronal clusters carried, on average, 0.03 bits of information about the stimulus on trials in which the rat's behavioral response was correct. To understand how cortical activity guides behavior, we examined responses in incorrect trials and found that, in contrast to correct trials, neuronal firing rate was higher for smooth than for rough textures. Analysis of high-speed films suggested that the inappropriate signal on incorrect trials was due, at least in part, to nonoptimal whisker contact. In conclusion, these data suggest that barrel cortex firing rate on each trial leads directly to the animal's judgment of texture

Spike timing in rat somatosensory cortex contributes to behavior

The precise spike timing of sensory neurons carries more information about stimuli than the number of spikes counted over longer time windows [1-3]. However, the behavioral relevance of this extra information remains to be assessed. To investigate whether precise timing contributes to behavior, we considered spike trains recorded extracellularly in the rat somatosensory cortex during a texture discrimination task [4,5]. We analyzed the spike trains following the contact of the whiskers with the texture and we measured the information carried about texture by post-touch spike times and spike counts. This analysis is technical challenging because it is difficult to quantify the information content of precise patterns of spike that extend over relatively long time windows with the relatively little number of trials available in behavioral experiments. To address this challenge, we reduced the dimensionality of the response space by decomposing single trial spike train densities into Principal Components (PCs), selecting the most informative PC as the "temporal template" to interpret neural responses, and finally measuring the information about the presented texture carried by the projection of each trial relative to this template. We compared the so -measured spike timing information with the information carried by spike counts and we found that spike times carried more than 60% more texture information than spike counts. Next, we reasoned that if a neuronal coding mechanism contributes to behavior, then the code would be found to transmit less stimulus information in error trials, i.e. trials in which the rat made the wrong choice. We found that the texture information carried both by spike counts and spike patterns decreased significantly when we included error trials in the analysis, but the effect was much more pronounced for patterns (30% information decrease) than for counts (~15% information decrease). These differences between spike pattern and spike count codes hold for both primary and secondary somatosensory cortex, suggesting that spike timing could contribute to behavior at different stages of the sensory processing. Taken together, these results indicate that in the somatosensory cortex the time at which spikes occur, not just the number of spikes, makes a crucial contribution to tactile perception

Psychometric Curve and Behavioral Strategies for Whisker-Based Texture Discrimination in Rats

The rodent whisker system is a major model for understanding neural mechanisms for tactile sensation of surface texture (roughness). Rats discriminate surface texture using the whiskers, and several theories exist for how texture information is physically sensed by the long, moveable macrovibrissae and encoded in spiking of neurons in somatosensory cortex. However, evaluating these theories requires a psychometric curve for texture discrimination, which is lacking. Here we trained rats to discriminate rough vs. fine sandpapers and grooved vs. smooth surfaces. Rats intermixed trials at macrovibrissa contact distance (nose >2 mm from surface) with trials at shorter distance (nose <2 mm from surface). Macrovibrissae were required for distant contact trials, while microvibrissae and non-whisker tactile cues were used for short distance trials. A psychometric curve was measured for macrovibrissa-based sandpaper texture discrimination. Rats discriminated rough P150 from smoother P180, P280, and P400 sandpaper (100, 82, 52, and 35 µm mean grit size, respectively). Use of olfactory, visual, and auditory cues was ruled out. This is the highest reported resolution for rodent texture discrimination, and constrains models of neural coding of texture information

Local circuits targeting parvalbumin-containing interneurons in layer IV of rat barrel cortex

Interactions between inhibitory interneurons and excitatory spiny neurons and also other inhibitory cells represent fundamental network properties which cause the so-called thalamo-cortical response transformation and account for the well-known receptive field differences of cortical layer IV versus thalamic neurons. We investigated the currently largely unknown morphological basis of these interactions utilizing acute slice preparations of barrel cortex in P19-21 rats. Layer IV spiny (spiny stellate, star pyramidal and pyramidal) neurons or inhibitory (basket and bitufted) interneurons were electrophysiologically characterized and intracellularly biocytin-labeled. In the same slice, we stained parvalbumin-immunoreactive (PV-ir) interneurons as putative target cells after which the tissue was subjected to confocal image acquisition. Parallel experiments confirmed the existence of synaptic contacts in these types of connection by correlated light and electron microscopy. The axons of the filled neurons differentially targeted barrel PV-ir interneurons: (1) The relative number of all contacted PV-ir cells within the axonal sphere was 5–17% for spiny (n = 10), 32 and 58% for basket (n = 2) and 12 and 13% for bitufted (n = 2) cells. (2) The preferential subcellular site which was contacted on PV-ir target cells was somatic for four and dendritic for five spiny cells; for basket cells, there was a somatic and for bitufted cells a dendritic preference in each examined case. (3) The highest number of contacts on a single PV-ir cell was 9 (4 somatic and 5 dendritic) for spiny neurons, 15 (10 somatic and 5 dendritic) for basket cells and 4 (1 somatic and 3 dendritic) for bitufted cells. These patterns suggest a cell type-dependent communication within layer IV microcircuits in which PV-ir interneurons provide not only feed-forward but also feedback inhibition thus triggering the thalamo-cortical response transformation