scholarly journals Two dynamically distinct circuits driving inhibition in sensory thalamus

2020 ◽  
Author(s):  
Rosa I. Martinez-Garcia ◽  
Bettina Voelcker ◽  
Julia B. Zaltsman ◽  
Saundra L. Patrick ◽  
Tanya R. Stevens ◽  
...  

AbstractMost sensory information destined for the neocortex is relayed through the thalamus, where considerable transformation occurs1,2. One powerful means of transformation involves interactions between excitatory thalamocortical neurons that carry data to cortex and inhibitory neurons of the thalamic reticular nucleus (TRN) that regulate flow of those data3-6. Despite enduring recognition of its importance7-9, understanding of TRN cell types, their organization, and their functional properties has lagged that of the thalamocortical systems they control.Here we address this, investigating somatosensory and visual circuits of the TRN. In the somatosensory TRN we observed two groups of genetically defined neurons that are topographically segregated, physiologically distinct, and connect reciprocally with independent thalamocortical nuclei via dynamically divergent synapses. Calbindin-expressing cells, located in the central core, connect with the ventral posterior nucleus (VP), the primary somatosensory thalamocortical relay. In contrast, somatostatin-expressing cells, residing along the surrounding edges of TRN, synapse with the posterior medial thalamic nucleus (POM), a higher-order structure that carries both top-down and bottom-up information10-12. The two TRN cell groups process their inputs in pathway-specific ways. Synapses from VP to central TRN cells transmit rapid excitatory currents that depress deeply during repetitive activity, driving phasic spike output. Synapses from POM to edge TRN cells evoke slower, less depressing excitatory currents that drive more persistent spiking. Differences in intrinsic physiology of TRN cell types, including state-dependent bursting, contribute to these output dynamics. Thus, processing specializations of two somatosensory TRN subcircuits appear to be tuned to the signals they carry—a primary central subcircuit to discrete sensory events, and a higher-order edge subcircuit to temporally distributed signals integrated from multiple sources. The structure and function of visual TRN subcircuits closely resemble those of the somatosensory TRN. These results provide fundamental insights about how subnetworks of TRN neurons may differentially process distinct classes of thalamic information.

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
B Semihcan Sermet ◽  
Pavel Truschow ◽  
Michael Feyerabend ◽  
Johannes M Mayrhofer ◽  
Tess B Oram ◽  
...  

Mouse primary somatosensory barrel cortex (wS1) processes whisker sensory information, receiving input from two distinct thalamic nuclei. The first-order ventral posterior medial (VPM) somatosensory thalamic nucleus most densely innervates layer 4 (L4) barrels, whereas the higher-order posterior thalamic nucleus (medial part, POm) most densely innervates L1 and L5A. We optogenetically stimulated VPM or POm axons, and recorded evoked excitatory postsynaptic potentials (EPSPs) in different cell-types across cortical layers in wS1. We found that excitatory neurons and parvalbumin-expressing inhibitory neurons received the largest EPSPs, dominated by VPM input to L4 and POm input to L5A. In contrast, somatostatin-expressing inhibitory neurons received very little input from either pathway in any layer. Vasoactive intestinal peptide-expressing inhibitory neurons received an intermediate level of excitatory input with less apparent layer-specificity. Our data help understand how wS1 neocortical microcircuits might process and integrate sensory and higher-order inputs.


2000 ◽  
Vol 83 (5) ◽  
pp. 2791-2801 ◽  
Author(s):  
Jed A. Hartings ◽  
Simona Temereanca ◽  
Daniel J. Simons

The thalamic reticular nucleus (Rt) is strategically positioned to integrate descending and ascending signals in the control of sensorimotor and other thalamocortical activity. Its prominent role in the generation of sleep spindles notwithstanding, relatively little is known of Rt function in regulating interactions with the sensory environment. We recorded and compared the responses of individual Rt and thalamocortical neurons in the ventroposterior medial (VPm) nucleus of the rat to controlled deflections of mystacial vibrissae. Transient Rt responses to the onset (on) and offset (off) of vibrissa deflection are larger and longer in duration than those of VPm and of all other populations studied in the whisker/barrel pathway. Magnitudes of on and off responses in Rt were negatively correlated with immediately preceding activities, suggesting a contribution of low-threshold T-type Ca2+ channels. Rt neurons also respond with high tonic firing rates during sustained vibrissa deflections. By comparison, VPm neurons are less likely to respond tonically and are more likely to exhibit tonic suppression. Rt and VPm populations are similar to each other, however, in that they retain properties of directional sensitivity established in primary afferent neurons. In both populations neurons are selective for deflection angle and exhibit directional consistency, responding best to a particular direction of movement regardless of the starting position of the vibrissal hair. These findings suggest a role for Rt in the processing of detailed sensory information. Temporally, Rt may function to limit the duration of stimulus-evoked VPm responses and to focus them on rapid vibrissa perturbations. Moreover, by regulating the baseline activity of VPm neurons, Rt may indirectly enhance the response selectivity of layer IV barrel neurons to synchronous VPm firing.


2007 ◽  
Vol 24 (6) ◽  
pp. 857-874 ◽  
Author(s):  
THOMAS FITZGIBBON ◽  
BRETT A. SZMAJDA ◽  
PAUL R. MARTIN

The thalamic reticular nucleus (TRN) supplies an important inhibitory input to the dorsal thalamus. Previous studies in non-primate mammals have suggested that the visual sector of the TRN has a lateral division, which has connections with first-order (primary) sensory thalamic and cortical areas, and a medial division, which has connections with higher-order (association) thalamic and cortical areas. However, the question whether the primate TRN is segregated in the same manner is controversial. Here, we investigated the connections of the TRN in a New World primate, the marmoset (Callithrix jacchus). The topography of labeled cells and terminals was analyzed following iontophoretic injections of tracers into the primary visual cortex (V1) or the dorsal lateral geniculate nucleus (LGNd). The results show that rostroventral TRN, adjacent to the LGNd, is primarily connected with primary visual areas, while the most caudal parts of the TRN are associated with higher order visual thalamic areas. A small region of the TRN near the caudal pole of the LGNd (foveal representation) contains connections where first (lateral TRN) and higher order visual areas (medial TRN) overlap. Reciprocal connections between LGNd and TRN are topographically organized, so that a series of rostrocaudal injections within the LGNd labeled cells and terminals in the TRN in a pattern shaped like rostrocaudal overlapping “fish scales.” We propose that the dorsal areas of the TRN, adjacent to the top of the LGNd, represent the lower visual field (connected with medial LGNd), and the more ventral parts of the TRN contain a map representing the upper visual field (connected with lateral LGNd).


2014 ◽  
Vol 34 (39) ◽  
pp. 13170-13182 ◽  
Author(s):  
S.-C. Lee ◽  
S. L. Patrick ◽  
K. A. Richardson ◽  
B. W. Connors

2019 ◽  
Author(s):  
Gil Vantomme ◽  
Zita Rovó ◽  
Romain Cardis ◽  
Elidie Béard ◽  
Georgia Katsioudi ◽  
...  

SummaryTo navigate in space, an animal must refer to sensory cues to orient and move. Circuit and synaptic mechanisms that integrate cues with internal head-direction (HD) signals remain, however, unclear. We identify an excitatory synaptic projection from the presubiculum (PreS) and the multisensory-associative retrosplenial cortex (RSC) to the anterodorsal thalamic reticular nucleus (TRN), so far classically implied in gating sensory information flow. In vitro, projections to TRN involved AMPA/NMDA-type glutamate receptors that initiated TRN cell burst discharge and feedforward inhibition of anterior thalamic nuclei. In vivo, chemogenetic anterodorsal TRN inhibition modulated PreS/RSC-induced anterior thalamic firing dynamics, broadened the tuning of thalamic HD cells, and led to preferential use of allo-over egocentric search strategies in the Morris water maze. TRN-dependent thalamic inhibition is thus an integral part of limbic navigational circuits wherein it coordinates external sensory and internal HD signals to regulate the choice of search strategies during spatial navigation.


2019 ◽  
Vol 15 (1) ◽  
pp. 451-479 ◽  
Author(s):  
Dara S. Manoach ◽  
Robert Stickgold

There is overwhelming evidence that sleep is crucial for memory consolidation. Patients with schizophrenia and their unaffected relatives have a specific deficit in sleep spindles, a defining oscillation of non-rapid eye movement (NREM) Stage 2 sleep that, in coordination with other NREM oscillations, mediate memory consolidation. In schizophrenia, the spindle deficit correlates with impaired sleep-dependent memory consolidation, positive symptoms, and abnormal thalamocortical connectivity. These relations point to dysfunction of the thalamic reticular nucleus (TRN), which generates spindles, gates the relay of sensory information to the cortex, and modulates thalamocortical communication. Genetic studies are beginning to provide clues to possible neurodevelopmental origins of TRN-mediated thalamocortical circuit dysfunction and to identify novel targets for treating the related memory deficits and symptoms. By forging empirical links in causal chains from risk genes to thalamocortical circuit dysfunction, spindle deficits, memory impairment, symptoms, and diagnosis, future research can advance our mechanistic understanding, treatment, and prevention of schizophrenia.


2007 ◽  
Vol 98 (5) ◽  
pp. 2903-2909 ◽  
Author(s):  
Ying-Wan Lam ◽  
S. Murray Sherman

The thalamic reticular nucleus is a layer of GABAergic neurons that occupy a strategic position between the thalamus and cortex. Here we used laser scanning photostimulation to compare in young mice (9–12 days old) the organization of the reticular inputs to first- and higher-order somatosensory relays, namely, the ventral posterior lateral nucleus and posterior nucleus, respectively. The reticulothalamic input footprints to the ventral posterior lateral nucleus neurons consisted of small, single, topographically organized elliptical regions in a tier away from the reticulothalamic border. In contrast, those to the posterior nucleus were complicated and varied considerably among neurons: although almost all contained a single elliptical region near the reticulothalamic border, in most cases, they consisted of additional discontinuous regions or relatively diffuse regions throughout the thickness of the thalamic reticular nucleus. Our results suggest two sources of reticular inputs to the posterior nucleus neurons: one that is relatively topographic from regions near the reticulothalamic border and one that is relatively diffuse and convergent from most or all of the thickness of the thalamic reticular nucleus. We propose that the more topographic reticular input is the basis of local inhibition seen in posterior nucleus neurons and that the more diffuse and convergent input may represent circuitry through which the ventral posterior lateral and posterior nuclei interact.


2020 ◽  
Author(s):  
Nadia Parmhans ◽  
Anne Drury Fuller ◽  
Eileen Nguyen ◽  
Katherine Chuang ◽  
David Swygart ◽  
...  

AbstractMembers of the POU4F/Brn3 transcription factor family have an established role in the development of retinal ganglion cell types (RGCs), the projection sensory neuron conveying visual information from the mammalian eye to the brain. Our previous work using sparse random recombination of a conditional knock-in reporter allele expressing Alkaline Phosphatase (AP) and intersectional genetics had identified three types of Pou4f3/Brn3c positive (Brn3c+) RGCs. Here, we describe a novel Brn3cCre mouse allele generated by serial Dre to Cre recombination. We use this allele to explore the expression overlap of Brn3c with Brn3a and Brn3b and the dendritic arbor morphologies and visual stimulus properties of Brn3c+ RGC types. Furthermore, we explore Brn3c-expressing brain nuclei. Our analysis reveals a much larger number of Brn3c+ RGCs and more diverse set of RGC types than previously reported. The majority of RGCs having expressed Brn3c during development are still Brn3c positive in the adult, and all of them express Brn3a while only about half express Brn3b. Intersection of Brn3b and Brn3c expression highlights an area of increased RGC density, similar to an area centralis, corresponding to part of the binocular field of view of the mouse. Brn3c+ neurons and projections are present in multiple brain nuclei. Brn3c+ RGC projections can be detected in the Lateral Geniculate Nucleus (LGN), Pretectal Area (PTA) and Superior Colliculus (SC) but also in the thalamic reticular nucleus (TRN), a visual circuit station that was not previously described to receive retinal input. Most Brn3c+ neurons of the brain are confined to the pretectum and the dorsal midbrain. Amongst theses we identify a previously unknown Brn3c+ subdivision of the deep mesencephalic nucleus (DpMe). Thus, our newly generated allele provides novel biological insights into RGC type classification, brain connectivity and midbrain cytoarchitectonic, and opens the avenue for specific characterization and manipulation of these structures.


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