scholarly journals Higher order thalamus encodes correct goal-directed action

2020 ◽  
Author(s):  
D. LaTerra ◽  
S. Petryszyn ◽  
Marius Rosier ◽  
L.M. Palmer

ABSTRACTThe thalamus is the gateway to the cortex. Cortical encoding of sensory information can therefore only be understood by considering the influence of thalamic processing on sensory input. Despite modulating sensory processing, little is known about the role of the thalamus during sensory-based behavior, let alone goal-directed behavior. Here, we use two-photon Ca2+ imaging, patch-clamp electrophysiology and optogenetics to investigate the role of axonal projections from the posteromedial nucleus of the thalamus (POm) to the forepaw area of the primary somatosensory cortex (forepaw S1) during sensory processing and goal-directed behavior. We demonstrate that POm axons are active during tactile stimulus and increase activity specifically during the response and, to a lesser extent, reward epochs of a tactile goal-directed task. Furthermore, POm axons in forepaw S1 preferentially signaled correct behavior, with greatest activity during HIT responses. This activity is important for behavioral performance, as photoinhibition of archaerhodopsin-expressing neurons in the POm decreased overall behavioral success. Direct juxtacelluar recordings in the awake state illustrates POm neurons fire sustained action potentials during tactile stimulus. This tactile-evoked POm firing pattern was used during ChR2 photoactivation of POm axons in forepaw S1, revealing that action potentials in layer 2/3 (L2/3) pyramidal neurons are inhibited during sustained POm input. Taken together, POm axonal projections in forepaw S1 encode correct goal-directed active behavior, leading to GABAA-mediated inhibition of L2/3 pyramidal neurons.

2021 ◽  
Vol 14 (1) ◽  
Author(s):  
Mingzhao Su ◽  
Junhua Liu ◽  
Baocong Yu ◽  
Kaixing Zhou ◽  
Congli Sun ◽  
...  

AbstractThe rodent whisker-barrel cortex system has been established as an ideal model for studying sensory information integration. The barrel cortex consists of barrel and septa columns that receive information input from the lemniscal and paralemniscal pathways, respectively. Layer 5a is involved in both barrel and septa circuits and play a key role in information integration. However, the role of layer 5a in the development of the barrel cortex remains unclear. Previously, we found that calretinin is dynamically expressed in layer 5a. In this study, we analyzed calretinin KO mice and found that the dendritic complexity and length of layer 5a pyramidal neurons were significantly decreased after calretinin ablation. The membrane excitability and excitatory synaptic transmission of layer 5a neurons were increased. Consequently, the organization of the barrels was impaired. Moreover, layer 4 spiny stellate cells were not able to properly gather, leading to abnormal formation of barrel walls as the ratio of barrel/septum size obviously decreased. Calretinin KO mice exhibited deficits in exploratory and whisker-associated tactile behaviors as well as social novelty preference. Our study expands our knowledge of layer 5a pyramidal neurons in the formation of barrel walls and deepens the understanding of the development of the whisker-barrel cortex system.


2021 ◽  
Author(s):  
Mingzhao Su ◽  
Junhua Liu ◽  
Baocong Yu ◽  
Kaixing Zhou ◽  
Congli Sun ◽  
...  

Abstract The rodent whisker-barrel cortex system has been established as an ideal model for studying sensory information integration. The barrel cortex consists of barrel and septa columns that receive information input from the lemniscal and paralemniscal pathways, respectively. L5a is involved in both barrel and septa circuits and play a key role in information integration. However, the role of L5a in the development of the barrel cortex remains unclear. Previously, we found that Calretinin is dynamically expressed in L5a. In this study, we analyzed Cr KO mice and found that the dendritic complexity and length of L5a pyramidal neurons were significantly decreased after Cr ablation. The membrane excitability and excitatory synaptic transmission of L5a neurons were increased. Consequently, the organization of the barrels was impaired. Moreover, L4 spiny stellate cells were not able to properly gather, leading to abnormal formation of barrel walls as the ratio of barrel/septum size obviously decreased. Cr KO mice exhibited deficits in exploratory and whisker-associated tactile behaviors as well as social novelty preference. Our study expands our knowledge of L5a pyramidal neurons in the formation of barrel walls and deepens the understanding of the development of the whisker-barrel cortex system.


2011 ◽  
Vol 106 (6) ◽  
pp. 2982-2991 ◽  
Author(s):  
Shiro Nakamura ◽  
Robert M. Bradley

Geniculate ganglion (GG) cell bodies of chorda tympani (CT), greater superficial petrosal (GSP), and posterior auricular (PA) nerves transmit orofacial sensory information to the rostral nucleus of the solitary tract. We have used whole cell recording to investigate the characteristics of the Na+ channels in isolated Fluorogold-labeled GG neurons that innervate different peripheral receptive fields. GG neurons expressed two classes of Na+ channels, TTX sensitive (TTX-S) and TTX resistant (TTX-R). The majority of GG neurons expressed TTX-R currents of different amplitudes. TTX-R currents were relatively small in 60% of the neurons but were large in 12% of the sampled population. In a further 28% of the neurons, TTX completely abolished all Na+ currents. Application of TTX completely inhibited action potential generation in all CT and PA neurons but had little effect on the generation of action potentials in 40% of GSP neurons. Most CT, GSP, and PA neurons stained positively with IB4, and 27% of the GSP neurons were capsaicin sensitive. The majority of IB4-positive GSP neurons with large TTX-R Na+ currents responded to capsaicin, whereas IB4-positive GSP neurons with small TTX-R Na+ currents were capsaicin insensitive. These data demonstrate the heterogeneity of GG neurons and indicate the existence of a subset of GSP neurons sensitive to capsaicin, usually associated with nociceptors. Since there are no reports of nociceptors in the GSP receptive field, the role of these capsaicin-sensitive neurons is not clear.


2010 ◽  
Vol 103 (3) ◽  
pp. 1147-1157 ◽  
Author(s):  
Akio Hirata ◽  
Manuel A. Castro-Alamancos

Neocortex network activity varies from a desynchronized or activated state typical of arousal to a synchronized or deactivated state typical of quiescence. Such changes are usually attributed to the effects of neuromodulators released in the neocortex by nonspecific activating systems originating in basal forebrain and brain stem reticular formation. As a result, the only role attributed to thalamocortical cells projecting to primary sensory areas, such as barrel cortex, is to transmit sensory information. However, thalamocortical cells can undergo significant changes in spontaneous tonic firing as a function of state, although the role of such variations is unknown. Here we show that the tonic firing level of thalamocortical cells, produced by cholinergic and noradrenergic stimulation of the somatosensory thalamus in urethane-anesthetized rats, controls neocortex activation and deactivation. Thus in addition to its well-known role in the relay of sensory information, the thalamus can control the state of neocortex activation, which may complement the established roles in this regard of basal forebrain and brain stem nuclei. Because of the topographical organization of primary thalamocortical pathways, this mechanism provides a means by which area-specific neocortical activation can occur, which may be useful for modality-specific sensory processing or selective attention.


2019 ◽  
Author(s):  
Lan Tang ◽  
Michael J. Higley

SummarySensory areas of the mammalian neocortex are thought to act as distribution hubs, transmitting information about the external environment to various cortical and subcortical structures in order to generate adaptive behavior. However, the exact role of cortical circuits in sensory perception remains unclear. Within primary visual cortex (V1), various populations of pyramidal neurons (PNs) send axonal projections to distinct targets, suggesting multiple cellular networks that may be independently engaged during the generation of behavior. Here, we investigated whether PN subpopulations differentially support sensory-guided performance by training mice in a visual detection task based on eyeblink conditioning. Applying 2-photon calcium imaging and optogenetic manipulation of anatomically-defined PNs in behaving animals, we show that layer 5 corticopontine neurons strongly encode task information and are selectively necessary for performance. These results contrast with recent observations of operant behavior showing a limited role for the neocortex in sensory detection. Instead, our findings support a model in which target-specific cortical subnetworks form the basis for adaptive behavior by directing relevant information to downstream brain areas. Overall, this work highlights the potential for neurons to form physically interspersed but functionally segregated networks capable of parallel, independent control of perception and behavior.


2008 ◽  
Vol 100 (2) ◽  
pp. 620-628 ◽  
Author(s):  
Sylvain Rheims ◽  
Alfonso Represa ◽  
Yehezkel Ben-Ari ◽  
Yuri Zilberter

The neonatal period is critical for seizure susceptibility, and neocortical networks are central in infantile epilepsies. We report that application of 4-aminopyridine (4-AP) to immature (P6–P9) neocortical slices generates layer-specific interictal seizures (IISs) that transform after recurrent seizures to ictal seizures (ISs). During IISs, cell-attached recordings show action potentials in interneurons and pyramidal cells in L5/6 and interneurons but not pyramidal neurons in L2/3. However, L2/3 pyramidal neurons also fire during ISs. Using single N-methyl-d-aspartate (NMDA) channel recordings for measuring the cell resting potential ( Em), we show that transition from IISs to ISs is associated with a gradual Em depolarization of L2/3 and L5/6 pyramidal neurons that enhances their excitability. Bumetanide, a NKCC1 co-transporter antagonist, inhibits generation of IISs and prevents their transformation to ISs, indicating the role excitatory GABA in epilepsies. Therefore deep layer neurons are more susceptible to seizures than superficial ones. The initiating phase of seizures is characterized by IISs generated in L5/6 and supported by activation of both L5/6 interneurons and pyramidal cells. IISs propagate to L2/3 via activation of L2/3 interneurons but not pyramidal cells, which are mostly quiescent at this phase. In superficial layers, a persistent increase in excitability of pyramidal neurons caused by Em depolarization is associated with a transition from largely confined GABAergic IIS to ictal events that entrain the entire neocortex.


2018 ◽  
Vol 115 (30) ◽  
pp. E7184-E7192 ◽  
Author(s):  
Efrat Katz ◽  
Ohad Stoler ◽  
Anja Scheller ◽  
Yana Khrapunsky ◽  
Sandra Goebbels ◽  
...  

Neocortical pyramidal neurons express several distinct subtypes of voltage-gated Na+ channels. In mature cells, Nav1.6 is the dominant channel subtype in the axon initial segment (AIS) as well as in the nodes of Ranvier. Action potentials (APs) are initiated in the AIS, and it has been proposed that the high excitability of this region is related to the unique characteristics of the Nav1.6 channel. Knockout or loss-of-function mutation of the Scn8a gene is generally lethal early in life because of the importance of this subtype in noncortical regions of the nervous system. Using the Cre/loxP system, we selectively deleted Nav1.6 in excitatory neurons of the forebrain and characterized the excitability of Nav1.6-deficient layer 5 pyramidal neurons by patch-clamp and Na+ and Ca2+ imaging recordings. We now report that, in the absence of Nav1.6 expression, the AIS is occupied by Nav1.2 channels. However, APs are generated in the AIS, and differences in AP propagation to soma and dendrites are minimal. Moreover, the channels that are expressed in the AIS still show a clear hyperpolarizing shift in voltage dependence of activation, compared with somatic channels. The only major difference between Nav1.6-null and wild-type neurons was a strong reduction in persistent sodium current. We propose that the molecular environment of the AIS confers properties on whatever Na channel subtype is present and that some other benefit must be conferred by the selective axonal presence of the Nav1.6 channel.


2021 ◽  
Author(s):  
Gwendolin Schoenfeld ◽  
Sepp Kollmorgen ◽  
Christopher M Lewis ◽  
Philipp Bethge ◽  
Anna Maria Reuss ◽  
...  

Learning goal-directed behaviours requires integration of separate information streams representing context, relevant stimuli and reward. Dendrites of pyramidal neurons are suitable sites for such integration, but it remains elusive how their responses adapt when an animal learns a new task. Here, we identify two distinct classes of dendritic responses that represent either contextual/sensory information or reward information and that differ in their task- and learning-related dynamics. Using longitudinal calcium imaging of apical dendritic tufts of L5 pyramidal neurons in mouse barrel cortex, we tracked dendritic activity across learning and analyzed both local dendritic branch signals and global apical tuft activity. During texture discrimination learning, sensory representations (including contextual and touch information) strengthened and converged on the reward-predicting tactile stimulus when mice became experts. In contrast, reward-associated responses were particularly strong in the naive condition and became less pronounced upon learning. When we blocked the representation of unexpected reward in naive animals with optogenetic inhibition, animals failed to learn until we released the block and learning proceeded normally. Our results suggest that reward signals in dendrites are essential for adjusting neuronal integration of converging inputs to facilitate adaptive behaviour.


2019 ◽  
Author(s):  
Alexia Bourgeois ◽  
Carole Guedj ◽  
Emmanuel Carrera ◽  
Patrik Vuilleumier

Selective attention is a fundamental cognitive function that guides behavior by selecting and prioritizing salient or relevant sensory information of our environment. Despite early evidence and theoretical proposal pointing to an implication of thalamic control in attention, most studies in the past two decades focused on cortical substrates, largely ignoring the contribution of subcortical regions as well as cortico-subcortical interactions. Here, we suggest a key role of the pulvinar in the selection of salient and relevant information via its involvement in priority maps computation. Prioritization may be achieved through a pulvinar- mediated generation of alpha oscillations, which may then modulate neuronal gain in thalamo-cortical circuits. Such mechanism might orchestrate the synchrony of cortico-cortical interaction, by rendering neural communication more effective, precise and selective. We propose that this theoretical framework will support a timely shift from the prevailing cortico- centric view of cognition to a more integrative perspective of thalamic contributions to attention and executive control processes.


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