Cross-modal responses in the primary visual cortex encode complex objects and correlate with tactile discrimination.

Cortical areas that directly receive sensory inputs from the thalamus were long thought to be exclusively dedicated to a single modality, originating separate labeled lines. In the past decade, however, several independent lines of research have demonstrated cross-modal responses in primary sensory areas. To investigate whether these responses represent behaviorally relevant information, we carried out neuronal recordings in the primary somatosensory cortex (S1) and primary visual cortex (V1) of rats as they performed whisker-based tasks in the dark. During the free exploration of novel objects, V1 and S1 responses carried comparable amounts of information about object identity. During execution of an aperture tactile discrimination task, tactile recruitment was slower and less robust in V1 than in S1. However, V1 tactile responses correlated significantly with performance across sessions. Altogether, the results support the notion that primary sensory areas have a preference for a given modality but can engage in meaningful cross-modal processing depending on task demand.

Changes in S1 neural responses during tactile discrimination learning.

In freely moving rats that are actively performing a discrimination task, single-unit responses in primary somatosensory cortex (S1) are strikingly different from responses to comparable tactile stimuli in immobile rats. For example, in the active discrimination context prestimulus response modulations are common, responses are longer in duration and more likely to be inhibited. To determine whether these differences emerge as rats learned a whisker-dependent discrimination task, we recorded single-unit S1 activity while rats learned to discriminate aperture-widths using their whiskers. Even before discrimination training began, S1 responses in freely moving rats showed many of the signatures of active responses, such as increased duration of response and prestimulus response modulations. As rats subsequently learned the discrimination task, single unit responses changed: more cortical units responded to the stimuli, neuronal sensory responses grew in duration, and individual neurons better predicted aperture-width. In summary, the operant behavioral context changes S1 tactile responses even in the absence of tactile discrimination, whereas subsequent width discrimination learning refines the S1 representation of aperture-width.

Processing of tactile information by the hippocampus.

The ability to detect unusual events occurring in the environment is essential for survival. Several studies have pointed to the hippocampus as a key brain structure in novelty detection, a claim substantiated by its wide access to sensory information through the entorhinal cortex and also distinct aspects of its intrinsic circuitry. Novelty detection is implemented by an associative match-mismatch algorithm involving the CA1 and CA3 hippocampal subfields that compares the stream of sensory inputs received by CA1 to the stored representation of spatiotemporal sequences in CA3. In some rodents, including the rat, the highly sensitive facial whiskers are responsible for providing accurate tactile information about nearby objects. Surprisingly, however, not much is known about how inputs from the whiskers reach CA1 and how they are processed therein. Using concurrent multielectrode neuronal recordings and chemical inactivation in behaving rats, we show that trigeminal inputs from the whiskers reach the CA1 region through thalamic and cortical relays associated with discriminative touch. Ensembles of hippocampal neurons also carry precise information about stimulus identity when recorded during performance in an aperture-discrimination task using the whiskers. We also found broad similarities between tactile responses of trigeminal stations and the hippocampus during different vigilance states (wake and sleep). Taken together, our results show that tactile information associated with fine whisker discrimination is readily available to the hippocampus for dynamic updating of spatial maps.

Neuronal activity in the primary somatosensory thalamocortical loop is modulated by reward contingency during tactile discrimination.

Delayed-response sensory discrimination is believed to require primary sensory thalamus and cortex for early stimulus identification and higher-order forebrain regions for the late association of stimuli with rewarded motor responses. Here we investigate neuronal responses in the rat primary somatosensory cortex (S1) and ventral posterior medial nucleus of the thalamus (VPM) during a tactile discrimination task that requires animals to associate two different tactile stimuli with two corresponding choices of spatial trajectory to be rewarded. To manipulate reward expectation, neuronal activity observed under regular reward contingency (CR) was compared with neuronal activity recorded during freely rewarded (FR) trials, in which animals obtained reward regardless of their choice of spatial trajectory. Across-trial firing rates of S1 and VPM neurons varied according to the reward contingency of the task. Analysis of neuronal ensemble activity by an artificial neural network showed that stimulus-related information in S1 and VPM increased from stimulus sampling to reward delivery in CR trials but decreased to chance levels when animals performed FR trials, when stimulus discrimination was irrelevant for task execution. Neuronal ensemble activity in VPM was only correlated with task performance during stimulus presentation. In contrast, S1 neuronal activity was highly correlated with task performance long after stimulus removal, a relationship that peaked during the 300 ms that preceded reward delivery. Together, our results indicate that neuronal activity in the primary somatosensory thalamocortical loop is strongly modulated by reward contingency.

Global forebrain dynamics predict rat behavioral states and their transitions.

The wake-sleep cycle, a spontaneous succession of global brain states that correspond to major overt behaviors, occurs in all higher vertebrates. The transitions between these states, at once rapid and drastic, remain poorly understood. Here, intracranial local field potentials (LFPs) recorded in the cortex, hippocampus, striatum, and thalamus were used to characterize the neurophysiological correlates of the rat wake-sleep cycle. By way of a new method for the objective classification and quantitative investigation of all major brain states, we demonstrate that global brain state transitions occur simultaneously across multiple forebrain areas as specific spectral trajectories with characteristic path, duration, and coherence bandwidth. During state transitions, striking changes in neural synchronization are effected by the prominent narrow-band LFP oscillations that mark state boundaries. Our results demonstrate that distant forebrain areas tightly coordinate the processing of neural information during and between global brain states, indicating a very high degree of functional integration across the entire wake-sleep cycle. We propose that transient oscillatory synchronization of synaptic inputs, which underlie the rapid switching of global brain states, may facilitate the exchange of information within and across brain areas at the boundaries of very distinct neural processing regimens.

Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas.

The discovery of experience-dependent brain reactivation during both slow-wave (SW) and rapid eye-movement (REM) sleep led to the notion that the consolidation of recently acquired memory traces requires neural replay during sleep. To date, however, several observations continue to undermine this hypothesis. To address some of these objections, we investigated the effects of a transient novel experience on the long-term evolution of ongoing neuronal activity in the rat forebrain. We observed that spatiotemporal patterns of neuronal ensemble activity originally produced by the tactile exploration of novel objects recurred for up to 48 h in the cerebral cortex, hippocampus, putamen, and thalamus. This novelty-induced recurrence was characterized by low but significant correlations values. Nearly identical results were found for neuronal activity sampled when animals were moving between objects without touching them. In contrast, negligible recurrence was observed for neuronal patterns obtained when animals explored a familiar environment. While the reverberation of past patterns of neuronal activity was strongest during SW sleep, waking was correlated with a decrease of neuronal reverberation. REM sleep showed more variable results across animals. In contrast with data from hippocampal place cells, we found no evidence of time compression or expansion of neuronal reverberation in any of the sampled forebrain areas. Our results indicate that persistent experience-dependent neuronal reverberation is a general property of multiple forebrain structures. It does not consist of an exact replay of previous activity, but instead it defines a mild and consistent bias towards salient neural ensemble firing patterns. These results are compatible with a slow and progressive process of memory consolidation, reflecting novelty-related neuronal ensemble relationships that seem to be context- rather than stimulus-specific. Based on our current and previous results, we propose that the two major phases of sleep play distinct and complementary roles in memory consolidation: pretranscriptional recall during SW sleep and transcriptional storage during REM sleep.

Contour integration in the primary visual cortex of the opossum.

To investigate whether contour integration is a generalized mammalian feature we studied single cells in V1 on the South-America opossum ( ), a plesiomorphic animal believed to retain basic characteristics of early mammals. We observed that when a cell's receptive field (RF) was masked (i.e. an artificial scotoma was produced), sweeping a long bar (several times the length of the RF) at the cell's preferred orientation elicited robust responses in many cells (28/103, or 27%). Therefore, some cells in the primary visual cortex of the opossum interpolate under conditions consistent with physical occlusion. The present results indicate that the property of contour integration appears to be a basic property of the mammalian visual system.