Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities

Hendry, S. H. C.; Jones, Edward G.; Emson, Piers C.; Lawson, David; Heizmann, Claus W.; Streit, P.

doi:10.1007/bf00247904

Cited by 480 publications

(273 citation statements)

References 34 publications

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Section: -D Endritic I Nhibitory and D Isinhibitory S Yn-apses (D Oubmentioning

confidence: 97%

“…PVB has been shown to be expressed mainly by chandelier and basket cells (DeFelipe et al 1989a;Hendry et al 1989;Fonseca et al 1993;Gabbott and Bacon 1996a). PVB-positive neurons in the cortex, as well as in other brain regions such as the striatum and the hippocampus, have been characterized electrophysiologically as 'fast-spiking' neurons that show: (a) repetitive firing by synaptic activation of depolarized potentials; (b) short duration action potentials with short duration after-hyperpolarizations; (c) relatively negative resting potentials; and (d) lower input resistance with respect to other neuronal subpopulations (Kawaguchi and Kubota 1995; Cauli et al 1997).…”

Section: Neuroanatomical Studies Of Cortical Interneuronsmentioning

confidence: 99%

“…This protein has been reported to be mainly expressed by double bouquet cells (Hendry et al 1989; DeFelipe et al 1990;Kubota et al 1994; del Rio and DeFelipe 1995;Gabbott and Bacon 1996a) as well as by some Cajal-Retzius neurons in layer I. CB-positive neurons in the cortex were found to correspond to 'low threshold spike' cells: characterized electrophysiologically by broad spikes, pronounced adaptation of firing frequency and low-threshold spikes upon depolarization by synaptic activation Kubota 1993, 1995 'Low threshold' neurons have been found to be selectively connected to each other through electrical synapses and thus proposed to play a role in generating synchronous inhibitory activity in the cortex (Gibson et al 1999). CB-positive neurons in the cortex have also been found to be the main target of extrinsic GABAergic projections from the diagonal band of Broca (Freund and Gulyas 1991) and to receive CR-positive synaptic contacts on their distal dendrites (Gabbott and Bacon 1996a).…”

Section: Neuroanatomical Studies Of Cortical Interneuronsmentioning

confidence: 99%

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GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder

Beneš

Berretta

2001

Neuropsychopharmacology

982

643

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Neurons that express the compound, ␥ -aminobutyric acid (GABA), are broadly present throughout the central nervous system, although telencephalic structures, such as the cerebral cortex, show the most abundant quantities of this neurotransmitter (Jones 1987). In the discussion that follows, the anatomy and physiology of various types of GABAergic interneurons in the cortex and hippocampus will be discussed and related to recent postmortem studies implicating this transmitter system in the pathophysiology of schizophrenia and bi- 25 , NO . 1 polar disorder and their treatment with neuroleptic drugs (for more comprehensive reviews on cortical and hippocampal neurons see: Hof et al. 1993;Freund and Buzsaki 1996;Somogyi et al. 1998). NEUROBIOLOGY OF GABAERGIC INTERNEURONSBased on Golgi-impregnation studies, Ramon y Cajal provided the first descriptions of several different morphological subtypes of interneurons in the cerebral cortex and hippocampus (Ramon y Cajal 1893, 1911. In more recent years, it has been shown that, with some overlap, different morphological subtypes also have distinct distributions, connectivity, neurochemistry, and electrophysiological properties (for reviews see Hof et al. 1993;Freund and Buzsaki 1996). It is interesting to note that every segment of a pyramidal neuron, such as the soma, dendritic branches and spines, and the initial axonal segment, receives dense GABAergic synaptic innervation (O'Kusky and Colonnier 1982;Hendry et al. 1983;Houser et al. 1983; Beaulieu et al. 1992; for reviews see Jones 1993;Freund and Buzsaki 1996). Even more interestingly, each of these segments appears to be innervated by distinct GABAergic neuronal subtypes (see below).These differences strongly suggest that each of these subtypes plays a fundamentally different role in physiological and pathological mechanisms. In the discussion that follows, cortical interneurons will be described first, since our most basic understanding of GABAergic cells is derived from these populations. In more recent years, however, similar characterizations of interneurons in hippocampus have emerged. Although these cells show some striking similarities to their cortical counterparts, there are also some unique features that distinguish them. For this reason, interneurons in the hippocampus are discussed separately. Cortex Neuroanatomical Studies of Cortical Interneurons.Various types of GABAergic neurons can be categorized according to the type of synaptic profiles they are associated with, as this has direct implications for understanding the physiological role of these cells in cortical circuits. These categories are discussed below.A XO -S OMATIC I NHIBITORY S YNAPSES (B ASKET C ELLS ). The most commonly encountered interneurons ( Figure 1A) are multipolar in shape, i.e., they may have three or more primary dendritic branches emanating from their cell bodies, some having somata that are as large as those of pyramidal neurons (Jones and Hendry 1984). Using immunocytochemistry to localize the enzyme ). These cells also ...

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Section: -D Endritic I Nhibitory and D Isinhibitory S Yn-apses (D Oubmentioning

confidence: 97%

Section: Neuroanatomical Studies Of Cortical Interneuronsmentioning

confidence: 99%

Section: Neuroanatomical Studies Of Cortical Interneuronsmentioning

confidence: 99%

See 1 more Smart Citation

GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder

Beneš

Berretta

2001

Neuropsychopharmacology

982

643

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“…Hendry et al, 1989;van Brederode et al, 1990;Lund and Lewis, 1993;Conde ¤ et al, 1994;Gabbott and Bacon, 1996;Yan et al, 1996). We conducted this analysis in cases with injections of £uorescent dyes and BDA in anterior temporal, medial prefrontal, orbitofrontal cortices, and the hypothalamus.…”

Section: Connections Of Anterior Temporal Cortices With the Amygdala:mentioning

confidence: 99%

Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey

2002

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AbstractöThe amygdala has been implicated in processing information about the emotional signi¢cance of the environment and in the expression of emotions, through robust pathways with prefrontal, anterior temporal areas, and central autonomic structures. We investigated the anatomic organization and intersection of these pathways in the amygdala in rhesus monkeys with the aid of bidirectional, retrograde and anterograde tracers. Connections of the amygdala with orbitofrontal and medial prefrontal areas were robust and bidirectional, whereas connections with lateral prefrontal areas were sparse, unidirectional and ascending. Orbitofrontal axons terminated densely in a narrow band around the borders of the magnocellular basolateral nucleus, surrounded by projection neurons along a continuum through the nuclei of the basal complex. In contrast, the input and output zones of medial prefrontal areas were intermingled in the amygdala. Moreover, medial prefrontal axonal terminations were expansive, spreading into the parvicellular basolateral nucleus, which is robustly connected with hypothalamic autonomic structures, suggesting that they may in£uence the expressive emotional system of the amygdala. On the other hand, orbitofrontal axons heavily targeted the intercalated masses, which issue inhibitory projections to the central nucleus, at least in rats and cats. The central nucleus, in turn, issues a signi¢cant inhibitory projection to hypothalamic and brainstem autonomic structures. This evidence suggests that orbitofrontal areas exercise control on the internal processing of the amygdala. In addition, the results provided direct evidence that the connections of anterior temporal visual and auditory association cortices occupy overlapping territories with the orbitofrontal cortices particularly in the posterior half of the amygdala, and speci¢cally within the intermediate sector of the basolateral nucleus and in the magnocellular part of the basomedial nucleus (also known as accessory basal), suggesting a closely linked triadic network. This intricate network may be recruited in cognitive tasks that are inextricably linked with emotional associations.

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“…In contrast, PVB/-/-and PVB/PNN/-neurons shared similar features, with the exception of their morphological profiles. We propose that such differences among subgroups of PVB-IR neurons might imply specialized functional roles.PVB-IR neurons in the BLC, as well as in other cortical and cortical-like regions, are GABAergic and tend to form clusters of synaptic terminals that surround the somata and proximal axon segments of projection neurons (DeFelipe et al, 1989;Hendry et al, 1989;Fonseca et al, 1993;Freund and Buzsaki, 1996;Gabbott and Bacon, 1996;Sorvari et al, 1996a;McDonald and Mascagni, 2001). In the BLC, these neurons have been shown to receive their main inputs from intrinsic projection neurons (Smith et al, 2000;McDonald et al, 2005).…”

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confidence: 99%

Subpopulations of neurons expressing parvalbumin in the human amygdala

Pantazopoulos

Lange

Hassinger

et al. 2006

J of Comparative Neurology

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Amygdalar intrinsic inhibitory networks comprise several subpopulations of γ-aminobutyric acidergic neurons, each characterized by distinct morphological features and clusters of functionally relevant neurochemical markers. In rodents, the calcium-binding proteins parvalbumin (PVB) and calbindin D28k (CB) are coexpressed in large subpopulations of amygdalar interneurons. PVBimmunoreactive (-IR) neurons have also been shown to be ensheathed by perineuronal nets (PNN), extracellular matrix envelopes believed to affect ionic homeostasis and synaptic plasticity. We tested the hypothesis that differential expression of these three markers may define distinct neuronal subpopulations within the human amygdala. Toward this end, triple-fluorescent labeling using antisera raised against PVB and CB as well as biotinylated Wisteria floribunda lectin for detection of PNN was combined with confocal microscopy. Among the 1,779 PVB-IR neurons counted, 18% also expressed CB, 31% were ensheathed in PNN, and 7% expressed both CB and PNN. Forty-four percent of PVB-IR neurons did not colocalize with either CB or PNN. The distribution of each of these neuronal subgroups showed substantial rostrocaudal gradients. Furthermore, distinct morphological features were found to characterize each neuronal subgroup. In particular, significant differences relative to the distribution and morphology were detected between PVB-IR neurons expressing CB and PVB-IR neurons wrapped in PNNs. These results indicate that amygdalar PVB-IR neurons can be subdivided into at least four different subgroups, each characterized by a specific neurochemical profile, morphological characteristics, and three-dimensional distribution. Such properties suggest that each of these neuronal subpopulations may play a specific role within the intrinsic circuitry of the amygdala. Keywordscalbindin D28k; perineuronal nets; immunocytochemistry; confocal microscopy; basolateral complex of the amygdala The basolateral complex of the amygdala (lateral, basolateral, and accessory basal nuclei; BLC) plays an important role in assigning affective and motivational significance to sensory inputs, forming emotional memories, and generating emotional responses (Gloor, 1986;Halgren, 1992;Brothers, 1990;LeDoux, 1992;Aggleton, 1993;Adolphs et al., 1994). Complex intrinsic inhibitory circuits are believed to represent a critical component of the neural networks NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript underlying these functions. Among the several subpopulations of interneurons forming these circuits, those expressing the calcium-binding protein parvalbumin (PVB) are localized preferentially within the BLC (Sorvari et al., 1995). These neurons have been shown to affect information processing in this region crucially. For instance, the extremely low spontaneous firing rates typical of BLC projection neurons are thought to be the result of strong intrinsic inhibitory pressures originating from PVB-immunoreactive (-IR) neurons (Rainnie et al., 1991;Par...

show abstract

Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities

Cited by 480 publications

References 34 publications

GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder

GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder

Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey

Subpopulations of neurons expressing parvalbumin in the human amygdala

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