Feed-forward information and zero-lag synchronization in the sensory thalamocortical circuit are modulated during stimulus perception (original) (raw)

Single-neuron interactions between the somatosensory thalamo-cortical circuits during perception

SUMMARYSensory thalamo-cortical interactions are key components of the neuronal chains associated with stimulus perception, but surprisingly, they are poorly understood. We addressed this problem by evaluating a directional measure between simultaneously recorded neurons from somatosensory thalamus (VPL) and somatosensory cortex (S1) sharing the same cutaneous receptive field, while monkeys judged the presence or absence of a tactile stimulus. During the stimulus-presence, feedforward (VPL→S1) interactions increased, while pure feedback (S1→VPL) interactions were unaffected. Remarkably, bidirectional interactions (VPL↔S1) emerged with high stimulus amplitude, establishing a functional thalamo-cortical loop. Furthermore, feedforward interactions were modulated by task context and error trials. Additionally, significant stimulus modulations were found on intra-cortical (S1→S1) interactions, but not on intra-thalamic (VPL→VPL) interactions. Thus, these results show the directionality o...

Thalamocortical interactions shape hierarchical neural variability during stimulus perception

The brain is hierarchically organized to process sensory signals. But, to what extent do functional connections within and across areas shape this hierarchical order? We addressed this problem in the thalamocortical network, while monkeys judged the presence or absence of a vibrotactile stimulus. We quantified the variability and a directed connectivity measure in simultaneously recorded neurons sharing the same cutaneous receptive field from the somatosensory thalamus (VPL) and areas 3b and 1 from the somatosensory cortex. During the stimulus presence, neuronal variability increased along the network VPL-3b-1. Furthermore, VPL and area 3b display fast dynamics with rapid feedforward interactions. In contrast, area 1 shows slower timescales with persistent intra-area interactions. Our results suggest that the lower variability of VPL and area 3b facilitates feedforward thalamocortical communication, while the higher variability of area 1 supports intra-cortical interactions during s...

Neural coding and perceptual detection in the primate somatosensory thalamus

Proceedings of the National Academy of Sciences, 2012

The contribution of the sensory thalamus to perception and decision making is not well understood. We addressed this problem by recording single neurons in the ventral posterior lateral (VPL) nucleus of the somatosensory thalamus while trained monkeys judged the presence or absence of a vibrotactile stimulus of variable amplitude applied to the skin of a fingertip. We found that neurons in the VPL nucleus modulated their firing rate as a function of stimulus amplitude, and that such modulations accounted for the monkeys' overall psychophysical performance. These neural responses did not predict the animals' decision reports in individual trials, however. Moreover, the sensitivity to changes in stimulus amplitude was similar when the monkeys' performed the detection task and when they were not required to report stimulus detection. These results suggest that the primate somatosensory thalamus likely provides a reliable neural representation of the sensory input to the cerebral cortex, where sensory information is transformed and combined with other cognitive components associated with behavioral performance.

Thalamocortical loops as temporal demodulators across senses

Communications Biology

Sensory information is coded in space and in time. The organization of neuronal activity in space maintains straightforward relationships with the spatial organization of the perceived environment. In contrast, the temporal organization of neuronal activity is not trivially related to external features due to sensor motion. Still, the temporal organization shares similar principles across sensory modalities. Likewise, thalamocortical circuits exhibit common features across senses. Focusing on touch, vision, and audition, we review their shared coding principles and suggest that thalamocortical systems include circuits that allow analogous recoding mechanisms in all three senses. These thalamocortical circuits constitute oscillations-based phase-locked loops, that translate temporally-coded sensory information to rate-coded cortical signals, signals that can integrate information across sensory and motor modalities. The loop also allows predictive locking to the onset of future modul...

Thalamic encoding of complex sensory patterns and its possible role in cognition

2020

The function of the higher-order sensory thalamus remains unresolved. Here, POm nucleus was examined by in vivo extracellular recordings across a range of complex sensory patterns. We found that POm was highly sensitive to multiwhisker stimuli involving complex spatiotemporal interactions. The dynamical spatiotemporal structure of sensory patterns and the different complexity of their parts were accurately reflected in precise POm activity changes. Importantly, POm was also able to respond to ipsilateral stimulation and was implicated in the representation of bilateral tactile events by integrating simultaneous signals arising from both whisker pads. We found that POm nuclei are mutually connected through the cortex forming a functional POm-POm loop. We unravelled the nature and content of the messages travelling through this loop showing that they were ‘structured patterns of sustained activity’. These structured messages were transmitted preserving their integrated structure. The ...

THALAMOCORTICA INTERACTIONS shape hierarchical neural variability during stimulus perception

iScience , 2024

The brain is organized hierarchically to process sensory signals. But, how do functional connections within and across areas contribute to this hierarchical order? We addressed this problem in the thalamocortical network, while monkeys detected vibrotactile stimulus. During this task, we quantified neural variability and directed functional connectivity in simultaneously recorded neurons sharing the cutaneous receptive field within and across VPL and areas 3b and 1. Before stimulus onset, VPL and area 3b exhibited similar fast dynamics while area 1 showed slower timescales. During the stimulus presence, inter-trial neural vari- ability increased along the network VPL-3b-1 while VPL established two main feedforward pathways with areas 3b and 1 to process the stimulus. This lower variability of VPL and area 3b was found to regulate feedforward thalamocortical pathways. Instead, intra-cortical interactions were only anticipated by higher intrinsic timescales in area 1. Overall, our results provide evidence of hierarchical functional roles along the thalamocortical network.

Cortical Function: A View from the Thalamus

Neuron, 2005

processing through the thalamus. As a result, even our assumptions about the linear processing of sensory inand Martha E. Bickford 4 formation to guide action should be questioned. 1 Department of Physiology The meeting emphasized three areas, each of which 2 Department of Ophthalmology and Visual Sciences inspire new thinking about thalamic function. The first 3 Department of Anatomy was the organization and dynamic nature of thalamo-University of Wisconsin-Madison Medical School cortical pathways. The second was the role of the thal-Madison, Wisconsin 53706 amus in communication between cortical areas. And 4 Department of Anatomical Sciences the third was the relationship between sensory and moand Neurobiology tor pathways of the brain, including cognitive aspects University of Louisville of thalamocortical processing. The three-day meeting School of Medicine was lively and spirited throughout, exploring novel Louisville, Kentucky 40292 views of the importance of the thalamus. For interested readers, the proceedings of the meeting will be published in Progress in Brain Research in 2005. Here we review the main themes of the meeting. Neuroscientists from across the country gathered at From the Periphery to Perception: Thalamic the University of Wisconsin, Madison in September Processing Is Dynamic to honor Ray Guillery and his seminal work on the How do we become aware of our environment, and how thalamus. The meeting focused on three timely redoes our brain sort the host of competing signals arissearch topics, each of which inspired new thinking ing from our sensory receptors? Awareness of the about thalamic function. Presentations on the organworld depends upon sensory information reaching the ization and dynamic nature of thalamocortical pathcerebral cortex. All sensory information (except olfacways, the role of the thalamus in communication betory) passes through the thalamus before it reaches the tween cortical areas, and the relationship between cortex. As a result, the thalamus can be expected to sensory and motor pathways of the brain, including play an important role in conscious perception. Howcognitive aspects of thalamocortical processing, ever, the nature of this role is just beginning to be recmade for lively discussions. The meeting revealed ognized. Historically, the thalamus was considered a that communication between thalamus and cortex is simple relay of sensory information to the cortex. If this so rich that we should no longer consider the operawere true, why have a thalamus at all? Why not have tions of either structure separately from the other. the primary sensory afferents project directly to the cor-Proceedings of the meeting will be published in Protex? A key point of the discussions at the meeting was gress in Brain Research in 2005. In this report, we that the thalamus is more than a passive relay. The thalprovide a general overview of the main themes of amus controls the flow of information to cortex. Speakthe meeting.

Coding perceptual discrimination in the somatosensory thalamus

Proceedings of the National Academy of Sciences, 2012

The sensory thalamus is classically viewed as a relay station of sensory information to cortex, but recent studies suggest that it is sensitive to cognitive demands. There are, however, few experiments designed to test whether this is so. We addressed this problem by analyzing the responses of single neurons recorded in the somatosensory thalamus while trained monkeys reported a decision based on the comparison of two mechanical vibration frequencies applied sequentially to one fingertip. In this task, monkeys must hold the first stimulus frequency (f1) in working memory and compare it to the current sensory stimulus (f2) and must postpone the decision report until a cue triggers the decision motor report, i.e., whether f2 > f1 or f2 < f1. We found that thalamic somatosensory neurons encoded the stimulus frequency either in their periodicity and firing-rate responses, but only during the stimulus periods and not during the working memory and decision components of this task. F...

Thalamocortical rhythms during a vibrotactile detection task

Proceedings of the National Academy of Sciences of the United States of America, 2014

To explore the role of oscillatory dynamics of the somatosensory thalamocortical network in perception and decision making, we recorded the simultaneous neuronal activity in the ventral posterolateral nucleus (VPL) of the somatosensory thalamus and primary somatosensory cortex (S1) in two macaque monkeys performing a vibrotactile detection task. Actively detecting a vibrotactile stimulus and reporting its perception elicited a sustained poststimulus beta power increase in VPL and an alpha power decrease in S1, in both stimulus-present and stimulus-absent trials. These oscillatory dynamics in the somatosensory thalamocortical network depended on the behavioral context: they were stronger for the active detection condition than for a passive stimulation condition. Furthermore, contrasting stimulus-present vs. stimulus-absent responses, we found that poststimulus theta power increased in both VPL and S1, and alpha/beta power decreased in S1, reflecting the monkey's perceptual decis...