scholarly journals Neurotransmitters in the Mammalian Striatum: Neuronal Circuits and Heterogeneity

Author(s):  
K. Semba ◽  
H.C. Fibiger ◽  
S.R. Vincent

ABSTRACT:The major input and output pathways of the mammalian striatum have been well established. Recent studies have identified a number of neurotransmitters used by these pathways as well as by striatal interneurons, and have begun to unravel their synaptic connections. The major output neurons have been identified as medium spiny neurons which contain ɣ-aminobutyric acid (GABA), endogeneous opioids, and substance P. These neurons project to the pallidum and substantia nigra in a topographic and probably chemically organized manner. The major striatal afferents from the cerebral cortex, thalamus, and substantia nigra terminate, at least in part, on these striatal projection neurons. Striatal interneurons contain acetylcholine, GABA, and somatostatin plus neuropeptide Y, and appear to synapse on striatal projection neurons. In recent years, much activity has been directed to the neurochemical and hodological heterogeneities which occur at a macroscopic level in the striatum. This has led to the concept of a patch-matrix organization in the striatum.

2020 ◽  
Author(s):  
Adrienne C. Loewke ◽  
Adelaide R. Minerva ◽  
Alexandra B. Nelson ◽  
Anatol C. Kreitzer ◽  
Lisa A. Gunaydin

ABSTRACTThe dorsomedial prefrontal cortex (dmPFC) has been linked to approach-avoidance behavior and decision-making under conflict, key neural computations thought to be altered in anxiety disorders. However, the heterogeneity of efferent prefrontal projections has obscured identification of the specific top-down neural pathways regulating these anxiety-related behaviors. While the dmPFC-amygdala circuit has long been implicated in controlling reflexive fear responses, recent work suggests that this circuit is less important for avoidance behavior. We hypothesized that dmPFC neurons projecting to the dorsomedial striatum (DMS) represent a subset of prefrontal neurons that robustly encode and drive approach-avoidance behavior. Using fiber photometry recording during the elevated zero maze (EZM) task, we show heightened neural activity in prefrontal and fronto-striatal projection neurons, but not fronto-amydalar projection neurons, during exploration of the anxiogenic open arms of the maze. Additionally, through pathway-specific optogenetics we demonstrate that this fronto-striatal projection preferentially excites postsynaptic D1 receptor-expressing medium spiny neurons in the DMS and bidirectionally controls avoidance behavior. We conclude that this striatal-projecting subpopulation of prefrontal neurons regulates approach-avoidance conflict, supporting a model for prefrontal control of defensive behavior in which the dmPFC-amygdala projection controls reflexive fear behavior and the dmPFC-striatum projection controls anxious avoidance behavior. Our findings identify this fronto-striatal circuit as a valuable therapeutic target for developing interventions to alleviate excessive avoidance behavior in anxiety disorders.


2013 ◽  
Vol 109 (2) ◽  
pp. 315-320 ◽  
Author(s):  
Thomas G. Hawking ◽  
Todor V. Gerdjikov

Dorsolateral striatum (DLS) is implicated in tactile perception and receives strong projections from somatosensory cortex. However, the sensory representations encoded by striatal projection neurons are not well understood. Here we characterized the contribution of DLS to the encoding of vibrotactile information in rats by assessing striatal responses to precise frequency stimuli delivered to a single vibrissa. We applied stimuli in a frequency range (45–90 Hz) that evokes discriminable percepts and carries most of the power of vibrissa vibration elicited by a range of complex fine textures. Both medium spiny neurons and evoked potentials showed tactile responses that were modulated by slow wave oscillations. Furthermore, medium spiny neuron population responses represented stimulus frequency on par with previously reported behavioral benchmarks. Our results suggest that striatum encodes frequency information of vibrotactile stimuli which is dynamically modulated by ongoing brain state.


2005 ◽  
Vol 93 (2) ◽  
pp. 1119-1126 ◽  
Author(s):  
Fatuel Tecuapetla ◽  
Luis Carrillo-Reid ◽  
Jaime N. Guzmán ◽  
Elvira Galarraga ◽  
José Bargas

This work investigated if diverse properties could be ascribed to evoked inhibitory postsynaptic currents (IPSCs) recorded on rat neostriatal neurons when field stimulation was delivered at two different locations: the globus pallidus (GP) and the neostriatum (NS). Previous work stated that stimulation in the GP could antidromically excite projection axons from medium spiny neurons. This maneuver would predominantly activate the inhibitory synapses that interconnect spiny cells. In contrast, intrastriatal stimulation would preferentially activate inhibitory synapses provided by interneurons. This study shows that, in fact, intensity-amplitude experiments are able to reveal different properties for IPSCs evoked from these two locations (GP and NS). In addition, while all IPSCs evoked from the GP were always sensitive to ω-conotoxin GVIA (CaV2.22.2 or N-channel blocker), one-half of the inhibition evoked from the NS exhibited little sensitivity to ω-conotoxin GVIA. Characteristically, all ω-conotoxin GVIA–insensitive IPSCs exhibited strong paired pulse depression, whereas ω-conotoxin GVIA–sensitive IPSCs evoked from either the GP or the NS could exhibit short-time depression or facilitation. ω-Agatoxin TK (CaV2.12.1+ or P/Q-channel blocker) blocked IPSCs evoked from both locations. Therefore 1) distinct inhibitory inputs onto projection neostriatal cells can be differentially stimulated with field electrodes; 2) N-type Ca2+ channels are not equally expressed in inhibitory terminals activated in the NS; and 3) synapses that interconnect spiny neurons use both N- and P/Q-type Ca2+ channels.


1997 ◽  
Vol 77 (1) ◽  
pp. 427-434 ◽  
Author(s):  
Gabriele Radnikow ◽  
Jutta Rohrbacher ◽  
Ulrich Misgeld

Radnikow, Gabriele, Jutta Rohrbacher, and Ulrich Misgeld. Heterogeneity in use-dependent depression of inhibitory postsynaptic potentials in the rat neostriatum in vitro. J. Neurophysiol. 77: 427–434, 1997. “Minimal stimulation” was applied to evoke responses in an “all-or-none” fashion in presumed medium spiny neurons of rat neostriatal slices in the presence of antagonists for glutamatergic excitation. For comparison, responses were evoked in the same cells by compound stimulation. Bicuculline (30 μM) blocked responses evoked by minimal stimulation, indicating that they were γ-aminobutyric acid-A (GABAA)-receptor-mediated inhibitory postsynaptic potentials (IPSPs), whereas responses evoked by compound stimulation were only reduced in amplitude. Likewise, R(−)baclofen (1–20 μM) blocked IPSPs evoked by minimal stimulation in all but one cell. On the contrary, responses evoked by compound stimulation were always reduced in amplitude but never blocked. Paired-pulse depression (PPD) of averaged responses to minimal and compound stimulation was observed at a stimulus interval of 300 ms. The GABAB receptor antagonist CGP55845A (0.5 μM) had no effect on PPD evoked by compound stimulation but abolished PPD evoked by minimal stimulation. In a second set of experiments, the two stimulation paradigms were used to evoke responses in neostriatal slices continuously bathed in R(−)baclofen (10–20 μM). In R(−)baclofen a strong PPD was evoked by minimal and by compound stimulation. The amplitude of the response to compound stimulation increased on application of CGP55845A (0.5 μM). At the same time, PPD evoked by compound stimulation decreased. On the contrary, IPSP amplitude and PPD evoked by minimal stimulation remained unchanged. We conclude that two types of GABAergic terminals exist in the rat neostriatum, only one of which is regulated by GABAB receptors. However, the other class of terminals, not regulated by GABAB receptors, displays a much more pronounced PPD.


2012 ◽  
Vol 108 (6) ◽  
pp. 1739-1751 ◽  
Author(s):  
Luis A. Tellez ◽  
Isaac O. Perez ◽  
Sidney A. Simon ◽  
Ranier Gutierrez

Neurons in the nucleus accumbens (NAc) have been shown to participate in several behavioral states, including feeding and sleep. However, it is not known if the same neuron participates in both states and, if so, how similar are the responses. In addition, since the NAc contains several cell types, it is not known if each type participates in the transitions associated with feeding and sleep. Such knowledge is important for understanding the interaction between two different neural networks. For these reasons we recorded ensembles of NAc neurons while individual rats volitionally transitioned between the following states: awake and goal directed, feeding, quiet-awake, and sleeping. We found that during both feeding and sleep states, the same neurons could increase their activity (be activated) or decrease their activity (be inactivated) by feeding and/or during sleep, thus indicating that the vast majority of NAc neurons integrate sleep and feeding signals arising from spatially distinct neural networks. In contrast, a smaller population was modulated by only one of the states. For the majority of neurons in either state, we found that when one population was excited, the other was inhibited, suggesting that they act as a local circuit. Classification of neurons into putative interneurons [fast-spiking interneurons (pFSI) and choline acetyltransferase interneurons (pChAT)] and projection medium spiny neurons (pMSN) showed that all three types are modulated by transitions to and from feeding and sleep states. These results show, for the first time, that in the NAc, those putative inhibitory interneurons respond similarly to pMSN projection neurons and demonstrate interactions between NAc networks involved in sleep and feeding.


2021 ◽  
Author(s):  
Zhaorong Chen ◽  
Zhi-Yu Zhang ◽  
Taorong Xie ◽  
Wen Zhang ◽  
Yaping Li ◽  
...  

SUMMARYDrinking behavior in rodents is characterized by stereotyped, rhythmic licking movement, which is regulated by the basal ganglia. It is unclear how direct and indirect pathways control the lick bout and individual lick event. We find that inactivating D1 and D2 receptors-expressing medium spiny neurons (MSNs) in the ventrolateral striatum (VLS) oppositely alters the number of licks in a bout. D1- and D2-MSNs exhibit similar patterns of lick sequence-related activity but different phases of oscillation time-locked to the lick cycle. On timescale of a lick cycle, transient inactivation of D1-MSNs during tongue protrusion reduces lick probability, whereas transient inactivation of D2-MSNs has no effect. On timescale of a lick bout, inactivation of D1-MSNs (D2-MSNs) causes rate increase (decrease) in a subset of basal ganglia output neurons that decrease firing during licking. Our results reveal the distinct roles of D1- and D2-MSNs in regulating licking at both coarse and fine timescales.


Author(s):  
Natalie M. Doig ◽  
J. Paul Bolam

The striatum (or caudate-putamen, or caudate nucleus and putamen in those species in which they are divided by the internal capsule) is the major division of the basal ganglia, a group of structures involved in a variety of processes, including movement and cognitive and mnemonic functions. The striatum consists of a population of principal neurons, the medium-sized, densely spiny neurons (MSNs)—accounting for up to 97% of all neurons depending on species—which are the projection neurons of the striatum, several populations of GABAergic interneurons, and a population of cholinergic interneurons. The principal afferents of the striatum are glutamatergic, are derived from the cortex and thalamus, and mainly innervate the spines of MSNs. The essential computation performed by the striatum is the decision about which MSNs will fire, the consequence of which is altered firing of basal ganglia output neurons, and hence the selection of the basal ganglia–associated behavior.


2015 ◽  
Vol 113 (3) ◽  
pp. 843-855 ◽  
Author(s):  
Morgane Pidoux ◽  
Tejapratap Bollu ◽  
Tori Riccelli ◽  
Jesse H. Goldberg

Across species, complex circuits inside the basal ganglia (BG) converge on pallidal output neurons that exhibit movement-locked firing patterns. Yet the origins of these firing patterns remain poorly understood. In songbirds during vocal babbling, BG output neurons homologous to those found in the primate internal pallidal segment are uniformly activated in the tens of milliseconds prior to syllable onsets. To test the origins of this remarkably homogenous BG output signal, we recorded from diverse upstream BG cell types during babbling. Prior to syllable onsets, at the same time that internal pallidal segment-like neurons were activated, putative medium spiny neurons, fast spiking and tonically active interneurons also exhibited transient rate increases. In contrast, pallidal neurons homologous to those found in primate external pallidal segment exhibited transient rate decreases. To test origins of these signals, we performed recordings following lesion of corticostriatal inputs from premotor nucleus HVC. HVC lesions largely abolished these syllable-locked signals. Altogether, these findings indicate a striking homogeneity of syllable timing signals in the songbird BG during babbling and are consistent with a role for the indirect and hyperdirect pathways in transforming cortical inputs into BG outputs during an exploratory behavior.


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