scholarly journals High-order thalamic inputs to primary somatosensory cortex are stronger and longer lasting than cortical inputs

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Wanying Zhang ◽  
Randy M Bruno

Layer (L) 2/3 pyramidal neurons in the primary somatosensory cortex (S1) are sparsely active, spontaneously and during sensory stimulation. Long-range inputs from higher areas may gate L2/3 activity. We investigated their in vivo impact by expressing channelrhodopsin in three main sources of feedback to rat S1: primary motor cortex, secondary somatosensory cortex, and secondary somatosensory thalamic nucleus (the posterior medial nucleus, POm). Inputs from cortical areas were relatively weak. POm, however, more robustly depolarized L2/3 cells and, when paired with peripheral stimulation, evoked action potentials. POm triggered not only a stronger fast-onset depolarization but also a delayed all-or-none persistent depolarization, lasting up to 1 s and exhibiting alpha/beta-range oscillations. Inactivating POm somata abolished persistent but not initial depolarization, indicating a recurrent circuit mechanism. We conclude that secondary thalamus can enhance L2/3 responsiveness over long periods. Such timescales could provide a potential modality-specific substrate for attention, working memory, and plasticity.

2018 ◽  
Author(s):  
Elaine Zhang ◽  
Randy M Bruno

Layer (L) 2/3 pyramidal neurons in the primary somatosensory cortex (S1) are sparsely active, spontaneously and during sensory stimulation. Long-range inputs from higher areas may gate L2/3 activity. We investigated their in vivo impact by expressing channelrhodopsin in three main sources of feedback to rat S1: primary motor cortex, secondary somatosensory cortex, and secondary somatosensory thalamic nucleus (the posterior medial nucleus, POm). Inputs from cortical areas were relatively weak. POm, however, more robustly depolarized L2/3 cells and, when paired with peripheral stimulation, evoked action potentials. POm triggered not only a stronger fast-onset depolarization but also a delayed all-or-none persistent depolarization, lasting up to 1 second and exhibiting beta oscillations. Inactivating POm somata abolished persistent but not initial depolarization, indicating a recurrent circuit mechanism. We conclude that secondary thalamus can enhance L2/3 responsiveness over long periods. Such timescales could provide a potential modality-specific substrate for attention, working memory, and plasticity.


2016 ◽  
Vol 116 (3) ◽  
pp. 1261-1274 ◽  
Author(s):  
Amanda K. Kinnischtzke ◽  
Erika E. Fanselow ◽  
Daniel J. Simons

The functional role of input from the primary motor cortex (M1) to primary somatosensory cortex (S1) is unclear; one key to understanding this pathway may lie in elucidating the cell-type specific microcircuits that connect S1 and M1. Recently, we discovered that a subset of pyramidal neurons in the infragranular layers of S1 receive especially strong input from M1 (Kinnischtzke AK, Simons DJ, Fanselow EE. Cereb Cortex 24: 2237–2248, 2014), suggesting that M1 may affect specific classes of pyramidal neurons differently. Here, using combined optogenetic and retrograde labeling approaches in the mouse, we examined the strengths of M1 inputs to five classes of infragranular S1 neurons categorized by their projections to particular cortical and subcortical targets. We found that the magnitude of M1 synaptic input to S1 pyramidal neurons varies greatly depending on the projection target of the postsynaptic neuron. Of the populations examined, M1-projecting corticocortical neurons in L6 received the strongest M1 inputs, whereas ventral posterior medial nucleus-projecting corticothalamic neurons, also located in L6, received the weakest. Each population also possessed distinct intrinsic properties. The results suggest that M1 differentially engages specific classes of S1 projection neurons, thereby regulating the motor-related influence S1 exerts over subcortical structures.


2020 ◽  
Author(s):  
Nari Kim ◽  
Sangkyu Bahn ◽  
Joon Ho Choi ◽  
Jinseop S. Kim ◽  
Jong-Cheol Rah

ABSTRACTThe posterior medial nucleus of the thalamus (POm) and vibrissal primary motor cortex (vM1) convey essential information to the barrel cortex (S1BF) regarding whisker position and movement. Therefore, understanding the relative spatial relationships of these two inputs is critical prerequisites to acquire insight into how S1 synthesizes information to interpret the location of an object. Using array tomography, we identified the locations of synapses from vM1 and POm on distal tuft dendrites of L5 pyramidal neurons. We found that synapses from vM1 and POm are spatially clustered on the same set of dendrites with unusually high density. Furthermore, the clusters of vM1 and POm synapses colocalize each other. These findings suggest that synaptic clusters, but not dendritic branches, act as functional units and cooperatively contribute to nonlinear dendritic responses.


2015 ◽  
Vol 114 (3) ◽  
pp. 1652-1676 ◽  
Author(s):  
Miguel Pais-Vieira ◽  
Carolina Kunicki ◽  
Po-He Tseng ◽  
Joel Martin ◽  
Mikhail Lebedev ◽  
...  

Tactile information processing in the rodent primary somatosensory cortex (S1) is layer specific and involves modulations from both thalamocortical and cortico-cortical loops. However, the extent to which these loops influence the dynamics of the primary somatosensory cortex while animals execute tactile discrimination remains largely unknown. Here, we describe neural dynamics of S1 layers across the multiple epochs defining a tactile discrimination task. We observed that neuronal ensembles within different layers of the S1 cortex exhibited significantly distinct neurophysiological properties, which constantly changed across the behavioral states that defined a tactile discrimination. Neural dynamics present in supragranular and granular layers generally matched the patterns observed in the ventral posterior medial nucleus of the thalamus (VPM), whereas the neural dynamics recorded from infragranular layers generally matched the patterns from the posterior nucleus of the thalamus (POM). Selective inactivation of contralateral S1 specifically switched infragranular neural dynamics from POM-like to those resembling VPM neurons. Meanwhile, ipsilateral M1 inactivation profoundly modulated the firing suppression observed in infragranular layers. This latter effect was counterbalanced by contralateral S1 block. Tactile stimulus encoding was layer specific and selectively affected by M1 or contralateral S1 inactivation. Lastly, causal information transfer occurred between all neurons in all S1 layers but was maximal from infragranular to the granular layer. These results suggest that tactile information processing in the S1 of awake behaving rodents is layer specific and state dependent and that its dynamics depend on the asynchronous convergence of modulations originating from ipsilateral M1 and contralateral S1.


2019 ◽  
Vol 121 (1) ◽  
pp. 152-162 ◽  
Author(s):  
Nicholas Paul Holmes ◽  
Luigi Tamè

Transcranial magnetic stimulation (TMS) over human primary somatosensory cortex (S1), unlike over primary motor cortex (M1), does not produce an immediate, objective output. Researchers must therefore rely on one or more indirect methods to position the TMS coil over S1. The “gold standard” method of TMS coil positioning is to use individual functional and structural magnetic resonance imaging (f/sMRI) alongside a stereotactic navigation system. In the absence of these facilities, however, one common method used to locate S1 is to find the scalp location that produces twitches in a hand muscle (e.g., the first dorsal interosseus, M1-FDI) and then move the coil posteriorly to target S1. There has been no systematic assessment of whether this commonly reported method of finding the hand area of S1 is optimal. To do this, we systematically reviewed 124 TMS studies targeting the S1 hand area and 95 fMRI studies involving passive finger and hand stimulation. Ninety-six TMS studies reported the scalp location assumed to correspond to S1-hand, which was on average 1.5–2 cm posterior to the functionally defined M1-hand area. Using our own scalp measurements combined with similar data from MRI and TMS studies of M1-hand, we provide the estimated scalp locations targeted in these TMS studies of the S1-hand. We also provide a summary of reported S1 coordinates for passive finger and hand stimulation in fMRI studies. We conclude that S1-hand is more lateral to M1-hand than assumed by the majority of TMS studies.


2021 ◽  
Vol 15 ◽  
Author(s):  
Anders Wahlbom ◽  
Hannes Mogensen ◽  
Henrik Jörntell

We have previously reported different spike firing correlation patterns among pairs of adjacent pyramidal neurons within the same layer of S1 cortex in vivo, which was argued to suggest that acquired synaptic weight modifications would tend to differentiate adjacent cortical neurons despite them having access to near-identical afferent inputs. Here we made simultaneous single-electrode loose patch-clamp recordings from 14 pairs of adjacent neurons in the lateral thalamus of the ketamine-xylazine anesthetized rat in vivo to study the correlation patterns in their spike firing. As the synapses on thalamic neurons are dominated by a high number of low weight cortical inputs, which would be expected to be shared for two adjacent neurons, and as far as thalamic neurons have homogenous membrane physiology and spike generation, they would be expected to have overall similar spike firing and therefore also correlation patterns. However, we find that across a variety of thalamic nuclei the correlation patterns between pairs of adjacent thalamic neurons vary widely. The findings suggest that the connectivity and cellular physiology of the thalamocortical circuitry, in contrast to what would be expected from a straightforward interpretation of corticothalamic maps and uniform intrinsic cellular neurophysiology, has been shaped by learning to the extent that each pair of thalamic neuron has a unique relationship in their spike firing activity.


1993 ◽  
Vol 70 (3) ◽  
pp. 985-996 ◽  
Author(s):  
L. D. Lin ◽  
G. M. Murray ◽  
B. J. Sessle

1. Studies using ablation, intracortical microstimulation (ICMS) and surface stimulation, and single-neuron recordings have suggested that the primate primary somatosensory cortex (SI) may play an important role in movement control. Our aim was to determine whether bilateral inactivation of face SI would indeed interfere with the control of tongue or jaw-closing movements. 2. Effects of reversible inactivation by cooling of face SI was investigated in two monkeys trained to perform both a tongue-protrusion task and a biting task. The cooling experiments were carried out after the orofacial representation within SI was identified by systematically defining the mechanoreceptive field of single neurons recorded in face SI. The deficits in the tongue or jaw-closing movement were evaluated by the success rates for the monkeys' performance of both tasks and by the force and electromyographic (EMG) activity recorded from the masseter, genioglossus, and digastric muscles associated with the tasks. 3. During bilateral cooling of face SI, there was a statistically significant reduction in the success rates for the performance of the tongue-protrusion task in comparison with control series of trials while the thermodes used to cool face SI were kept at 37 degrees C. Detailed analyses of force and EMG activity showed that the principal deficit was the inability of the monkeys to maintain a steady tongue-protrusive force in the force holding period during each trial and to exert a consistent tongue-protrusion force between different trials. The task performance returned to control protocol levels at 4 min after commencement of rewarming. 4. Identical cooling conditions did not significantly affect the success rates for the performance of the biting task. Although the extent of the deficit was not severe enough to cause a significant reduction in successful rates for the biting task, cooling did significantly affect the ability of the monkeys to maintain a steady force in the holding period during each trial and to exert a consistent force between different trials. In one monkey the success rate of the biting task was also not affected by bilaterally cooling of face SI with a pair of larger thermodes placed on the dura over most of the face SI, face primary motor cortex (face MI), and adjacent cortical regions.(ABSTRACT TRUNCATED AT 400 WORDS)


eLife ◽  
2022 ◽  
Vol 11 ◽  
Author(s):  
Giacomo Ariani ◽  
J Andrew Pruszynski ◽  
Jörn Diedrichsen

Motor planning plays a critical role in producing fast and accurate movement. Yet, the neural processes that occur in human primary motor and somatosensory cortex during planning, and how they relate to those during movement execution, remain poorly understood. Here we used 7T functional magnetic resonance imaging (fMRI) and a delayed movement paradigm to study single finger movement planning and execution. The inclusion of no-go trials and variable delays allowed us to separate what are typically overlapping planning and execution brain responses. Although our univariate results show widespread deactivation during finger planning, multivariate pattern analysis revealed finger-specific activity patterns in contralateral primary somatosensory cortex (S1), which predicted the planned finger action. Surprisingly, these activity patterns were as informative as those found in contralateral primary motor cortex (M1). Control analyses ruled out the possibility that the detected information was an artifact of subthreshold movements during the preparatory delay. Furthermore, we observed that finger-specific activity patterns during planning were highly correlated to those during execution. These findings reveal that motor planning activates the specific S1 and M1 circuits that are engaged during the execution of a finger press, while activity in both regions is overall suppressed. We propose that preparatory states in S1 may improve movement control through changes in sensory processing or via direct influence of spinal motor neurons.


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