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2022 ◽  
Vol 15 ◽  
Author(s):  
Alexandra Tsolias ◽  
Maria Medalla

Acetylcholine (ACh) can act on pre- and post-synaptic muscarinic receptors (mAChR) in the cortex to influence a myriad of cognitive processes. Two functionally-distinct regions of the prefrontal cortex—the lateral prefrontal cortex (LPFC) and the anterior cingulate cortex (ACC)—are differentially innervated by ascending cholinergic pathways yet, the nature and organization of prefrontal-cholinergic circuitry in primates are not well understood. Using multi-channel immunohistochemical labeling and high-resolution microscopy, we found regional and laminar differences in the subcellular localization and the densities of excitatory and inhibitory subpopulations expressing m1 and m2 muscarinic receptors, the two predominant cortical mAChR subtypes, in the supragranular layers of LPFC and ACC in rhesus monkeys (Macaca mulatta). The subset of m1+/m2+ expressing SMI-32+ pyramidal neurons labeled in layer 3 (L3) was denser in LPFC than in ACC, while m1+/m2+ SMI-32+ neurons co-expressing the calcium-binding protein, calbindin (CB) was greater in ACC. Further, we found between-area differences in laminar m1+ dendritic expression, and m2+ presynaptic localization on cortico-cortical (VGLUT1+) and sub-cortical inputs (VGLUT2+), suggesting differential cholinergic modulation of top-down vs. bottom-up inputs in the two areas. While almost all inhibitory interneurons—identified by their expression of parvalbumin (PV+), CB+, and calretinin (CR+)—expressed m1+, the localization of m2+ differed by subtype and area. The ACC exhibited a greater proportion of m2+ inhibitory neurons compared to the LPFC and had a greater density of presynaptic m2+ localized on inhibitory (VGAT+) inputs targeting proximal somatodendritic compartments and axon initial segments of L3 pyramidal neurons. These data suggest a greater capacity for m2+-mediated cholinergic suppression of inhibition in the ACC compared to the LPFC. The anatomical localization of muscarinic receptors on ACC and LPFC micro-circuits shown here contributes to our understanding of diverse cholinergic neuromodulation of functionally-distinct prefrontal areas involved in goal-directed behavior, and how these interactions maybe disrupted in neuropsychiatric and neurological conditions.


2021 ◽  
Author(s):  
Varun Sreenivasan ◽  
Eleni Serafeimidou-Pouliou ◽  
David Exposito-Alonso ◽  
Kinga Bercsenyi ◽  
Clémence Bernard ◽  
...  

The assembly of functional neuronal circuits requires appropriate numbers of distinct classes of neurons, but the mechanisms through which their relative proportions are established remain poorly defined. Investigating the mouse striatum, here we found that the two most prominent subtypes of striatal interneurons, parvalbumin-expressing (PV+) GABAergic and cholinergic (ChAT+) interneurons, undergo extensive programmed cell death between the first and second postnatal weeks. Remarkably, the survival of PV+ and ChAT+ interneurons is regulated by distinct mechanisms mediated by their specific afferent connectivity. While long-range cortical inputs control PV+ interneuron survival, ChAT+ interneuron survival is regulated by local input from the medium spiny neurons. Our results identify input-specific circuit mechanisms that operate during the period of programmed cell death to establish the final number of interneurons in nascent striatal networks.


2021 ◽  
Author(s):  
Osnat Oz ◽  
Lior Matityahu ◽  
Aviv Mizrahi-Kliger ◽  
Alexander Kaplan ◽  
Noa Berkowitz ◽  
...  

The tonic activity of striatal cholinergic interneurons (CINs) is modified differentially by their afferent inputs. Although their unitary synaptic currents are identical, cortical inputs onto distal dendrites only weakly entrain CINs, whereas proximal thalamic inputs trigger abrupt pauses in discharge in response to salient external stimuli. To test whether the dendritic expression of the active conductances that drive autonomous discharge contribute to the CINs' capacity to dissociate cortical from thalamic inputs, we used an optogenetics-based method to quantify dendritic excitability. We found that the persistent sodium (NaP) current gave rise to dendritic boosting and that the hyperpolarization-activated cyclic nucleotide-gated (HCN) current gave rise to a subhertz membrane resonance. This resonance may underlie our novel finding of an association between CIN pauses and internally-generated slow wave events in sleeping non-human primates. Moreover, our method indicated that dendritic NaP and HCN currents were preferentially expressed in proximal dendrites. We validated this non-uniform distribution with two-photon imaging of dendritic back-propagating action potentials, and by demonstrating boosting of thalamic, but not cortical, inputs by NaP currents. Thus, the localization of active dendritic conductances in CIN dendrites mirrors the spatial distribution of afferent terminals and may promote their differential responses to thalamic vs. cortical inputs.


2021 ◽  
Author(s):  
Ayoub J Khalil ◽  
Huib Mansvelder ◽  
Laurens Witter

The basilar pontine nuclei (bPN) receive inputs from the entire neocortex and constitute the main source of mossy fibers to the cerebellum. Despite their critical position in the cortico-cerebellar pathway, it remains unclear if and how the bPN process inputs. An important unresolved question is whether the bPN strictly receives excitatory inputs or also receives inhibitory inputs. In the present study, we identified the mesodiencephalic junction as a prominent source of GABAergic afferents to the bPN. We combined optogenetics and whole-cell patch clamp recordings and confirmed that the bPN indeed receives monosynaptic GABA inputs from this region. Furthermore, we found no evidence that these inhibitory inputs converge with motor cortex (M1) inputs at the single neuron level. We also found no evidence of any connectivity between bPN neurons, suggesting the absence of a local circuit. Finally, rabies tracings revealed that GABAergic MDJ neurons themselves receive prominent inputs from neocortical output neurons. Our data indicates that inhibition from the MDJ, and excitation from the neocortex remain separate streams of information through the bPN. It is therefore unlikely that inhibition in the bPN has a gating function, but rather shapes an appropriate output of the bPN during behavior.


2021 ◽  
Author(s):  
Chia-wei Chang ◽  
Meiling Zhao ◽  
Samantha Grudzien ◽  
Max F Oginsky ◽  
Yexin Yang ◽  
...  

The primary somatosensory cortex (S1) is important for the control of movement as it encodes sensory input from the body periphery and external environment during ongoing movement. Mouse S1 consists of several distinct sensorimotor subnetworks that receive topographically organized cortico-cortical inputs from distant sensorimotor areas, including the secondary somatosensory cortex (S2) and primary motor cortex (M1). The role of the vibrissal S1 area and associated cortical connections during active sensing is well documented, but whether (and if so, how) non-whisker S1 areas are involved in movement control remains relatively unexplored. Here, we demonstrate that unilateral silencing of the non-whisker S1 area in both male and female mice disrupts hind paw movement during locomotion on a rotarod and a runway. S2 and M1 provide major long range inputs to this S1 area. Silencing S2 to non whisker S1 projections alters the hind paw orientation during locomotion while manipulation of the M1 projection has little effect. Using patch clamp recordings in brain slices from male and female mice, we show that S2 projection preferentially innervates inhibitory interneuron subtypes. We conclude that S2 S1 corticocortical interactions mediated by local interneurons are critical for efficient locomotion.


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.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Nora L. Benavidez ◽  
Michael S. Bienkowski ◽  
Muye Zhu ◽  
Luis H. Garcia ◽  
Marina Fayzullina ◽  
...  

AbstractThe superior colliculus (SC) receives diverse and robust cortical inputs to drive a range of cognitive and sensorimotor behaviors. However, it remains unclear how descending cortical input arising from higher-order associative areas coordinate with SC sensorimotor networks to influence its outputs. Here, we construct a comprehensive map of all cortico-tectal projections and identify four collicular zones with differential cortical inputs: medial (SC.m), centromedial (SC.cm), centrolateral (SC.cl) and lateral (SC.l). Further, we delineate the distinctive brain-wide input/output organization of each collicular zone, assemble multiple parallel cortico-tecto-thalamic subnetworks, and identify the somatotopic map in the SC that displays distinguishable spatial properties from the somatotopic maps in the neocortex and basal ganglia. Finally, we characterize interactions between those cortico-tecto-thalamic and cortico-basal ganglia-thalamic subnetworks. This study provides a structural basis for understanding how SC is involved in integrating different sensory modalities, translating sensory information to motor command, and coordinating different actions in goal-directed behaviors.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Behrad Noudoost ◽  
Kelsey Lynne Clark ◽  
Tirin Moore

Visually guided behavior relies on the integration of sensory input and information held in working memory (WM). Yet it remains unclear how this is accomplished at the level of neural circuits. We studied the direct visual cortical inputs to neurons within a visuomotor area of prefrontal cortex in behaving monkeys. We show that the efficacy of visual input to prefrontal cortex is gated by information held in WM. Surprisingly, visual input to prefrontal neurons was found to target those with both visual and motor properties, rather than preferentially targeting other visual neurons. Furthermore, activity evoked from visual cortex was larger in magnitude, more synchronous, and more rapid, when monkeys remembered locations that matched the location of visual input. These results indicate that WM directly influences the circuitry that transforms visual input into visually guided behavior.


2021 ◽  
Author(s):  
Alexandra Catherine McHale ◽  
Youngsun Teresa Cho ◽  
Julie Lynne Fudge

The prefrontal cortex (PFC) and insula, amygdala, and striatum form interconnected networks that drive motivated behaviors. We previously found a connectional trend in which granularity of the ventromedial and orbital PFC/insula predicted connections to the amygdala and also the scope of amygdalo-striatal efferents, including projections beyond the 'classic' ventral striatum. To further interrogate this triad and define the 'limbic (amygdala-recipient) striatum', we conducted tract tracing studies in two cohorts of primates to define the scope of cortico-amygdalo-striatal (indirect) and cortico-'limbic' striatal (direct) paths originating in the entire PFC and insula. With larger data sets and a quantitative approach, we found that the level of cortical granularity predicts the complexity and location of projections to both the amygdala and striatum. Remarkably, 'cortical-like' basal nucleus subdivisions also followed these rules in their projections to the striatum. In both 'direct' and 'indirect' paths to the 'limbic' striatum, agranular cortices formed a 'foundational', broad projection, and were joined by inputs from progressively more differentiated cortices. In amygdalo-striatal paths, the ventral basal nucleus was the 'foundational' input, with progressively more dorsal basal nucleus regions gradually adding inputs as the 'limbic striatum' extended caudally. Together, the 'indirect' and 'direct' paths follow consistent rules dictating projection strength and complexity to their targets. In the 'indirect' path, the agranular 'interoceptive' cortices consistently dominate amygdala inputs to the striatum. In contrast, 'direct' cortical inputs to the 'limbic' (amygdala-recipient) striatum create gradual shifts in connectivity fingerprints to provide clues to functional differences in the classic versus caudal ventral 'limbic' striatum.


2021 ◽  
Author(s):  
Emanuela Rizello ◽  
Sean Martin ◽  
Jennifer Rouine ◽  
Charlotte Callaghan ◽  
Shane O'Mara

Place cells are cells exhibiting location-dependent responses; they have mostly been studied in the hippocampus. Place cells have also been reported in the rat claustrum, an underexplored paracortical region with extensive corto-cortical connectivity. It has been hypothesised that claustral neuronal responses are anchored to cortical visual inputs. We show rat claustral place cells remap when visual inputs are eliminated from the environment and that this remapping is NMDA-receptor-dependent. Eliminating visual input enhances delta-band oscillatory activity in the claustrum, without affecting simultaneously-recorded visual cortical activity. We conclude that, like the hippocampus, claustral place field remapping might be mediated by NMDA receptor activity, and is modulated by visual cortical inputs.


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