The avian caudolateral neostriatum (NCL) was first identified on the basis of its dense dopaminergic innervation. This fact and data from lesion studies have led to the notion that NCL might be the avian equivalent of prefrontal cortex (PFC). A key feature of the PFC is the ability to integrate information from all modalities needed for the generation of motor plans. By using antero-and retrograde pathway tracing techniques, we investigated the organization of sensory afferents to the NCL and the connections with limbic and somatomotor centers in the basal ganglia and archistriatum. Data from all tracing experiments were compared with the distribution of tyrosine-hydroxylase (TH)-immunoreactive fibers, serving as a marker of dopaminergic innervation. The results show that NCL is reciprocally connected with the secondary sensory areas of all modalities and with at least two parasensory areas. Retrograde tracing also demonstrated further afferents from the deep layers of the Wulst and from the frontolateral neostriatum as well as the sources of thalamic input. Efferents of NCL project onto parts of the avian basal ganglia considered to serve somatomotor or limbic functions. Projections to the archistriatum are mainly directed to the somatomotor part of the intermediate archistriatum. In addition, cells in caudal NCL were found to be connected with the ventral and posterior archistriatum, which are considered avian equivalents of mammalian amygdala. All afferents and projection neurons were confined to the plexus of densest TH innervation. Our results show that the NCL is positioned to amalgamate information from all modalities and to exert control over limbic and somatomotor areas. This organization might comprise the neural basis for such complex behaviours as working memory or spatial orientation.
. Dopamine modulates excitability of basolateral amygdala neurons in vitro. J Neurophysiol 93: 1598 -1610, 2005. First published November 10, 2004; doi:10.1152/jn.00843.2004. The amygdala plays a role in affective behaviors, which are modulated by the dopamine (DA) innervation of the basolateral amygdala complex (BLA). Although in vivo studies indicate that activation of DA receptors alters BLA neuronal activity, it is unclear whether DA exerts direct effects on BLA neurons or whether it acts via indirect effects on BLA afferents. Using whole cell patch-clamp recordings in rat brain slices, we investigated the site and mechanisms through which DA regulates the excitability of BLA neurons. Dopamine enhanced the excitability of BLA projection neurons in response to somatic current injections via a postsynaptic effect. Dopamine D1 receptor activation increased excitability and evoked firing, whereas D2 receptor activation increased input resistance. Current-and voltage-clamp experiments in projection neurons showed that D1 receptor activation enhanced excitability by modulating a 4-aminopyridine-and ␣-dendrotoxin-sensitive, slowly inactivating K ϩ current. Furthermore, DA and D1 receptor activation increased evoked firing in fast-spiking BLA interneurons. Consistent with a postsynaptic modulation of interneuron excitability, DA also increased the frequency of spontaneous inhibitory postsynaptic currents recorded in projection neurons without changing release of GABA. These data demonstrate that DA exerts direct effects on BLA projection neurons and indirect actions via modulation of interneurons that may work in concert to enhance the neuronal response to large, suprathreshold inputs, while suppressing weaker inputs. Some of the enhancing effects of DA on affective behaviors may be explained by cellular actions of DA on BLA neurons. Systemic or iontophoretic administration of DA agonists alters the firing rate of BLA projection neurons and interneurons (Bashore et al. 1978; Ben-Ari and Kelly 1976;Rosenkranz and Grace 1999;Spehlmann and Norcross 1984). However, systemic administrations of DA receptor agonists also exert actions on synaptic inputs to the BLA Grace 2001, 2002a). Thus in these previous studies, it was difficult to exclude indirect effects of DA on BLA neurons via actions on afferent regions. Therefore in this study we utilized in vitro whole cell recordings from rat brain slices to test the hypothesis that DA exerts direct postsynaptic actions that alter BLA neuronal excitability, which could account for the effects observed in vivo with systemic administration of DA agonists, and to determine the receptor subtypes involved in these actions of DA.Our data show that DA increases the excitability of BLA projection neurons via mechanisms involving both D1 and D2 receptors and also increases evoked and spontaneous spike firing in fast-spiking interneurons. In projection neurons, the D1 receptor-dependent increase in excitability was due to the reduction in an outward-rectifying, 4-aminopyridine (4-AP) an...
In the primate neocortex, little is known about the possible associations between functional subclasses of GABA neurons, their morphological properties and calcium-binding protein (CaBP) content. We used whole-cell current clamp recordings, combined with intracellular labeling and fluorescence immunohistochemistry, to determine these relationships for interneurons in layers 2-3 of monkey prefrontal cortex (PFC). Eighty-one interneurons were included in the analysis. Thirty-eight of these cells showed immunoreactivity for one of the three CaBPs tested. Co-localization of more than one CaBP was not observed in any of the interneurons examined. Interneurons with different CaBPs formed distinct populations with specific physiological membrane properties and morphological features. Parvalbumin (PV)-positive cells had the physiological properties characteristic of fast-spiking interneurons (FS) and the morphology of basket or chandelier neurons. Most calretinin (CR)-containing cells had the physiological properties ascribed to non-fast-spiking cells (non-FS) and a vertically oriented axonal morphology, similar to that of double bouquet cells. Calbindin (CB)-positive interneurons also had non-FS properties and included cells with double bouquet morphology or with a characteristic dense web of axonal collaterals in layer 1. Classification of the interneurons based on cluster analysis of multiple electrophysiological properties suggested the existence of at least two distinct groups of interneurons. The first group contained mainly PV-positive FS cells and the second group consisted predominantly of CR- and CB-positive non-FS interneurons. These findings may help to illuminate the functional roles of different groups of interneurons in primate PFC circuitry.
In primates, little is known about intrinsic electrophysiological properties of neocortical neurons and their morphological correlates. To classify inhibitory cells (interneurons) in layers 2–3 of monkey dorsolateral prefrontal cortex we used whole cell voltage recordings and intracellular labeling in slice preparation with subsequent morphological reconstructions. Regular spiking pyramidal cells have been also included in the sample. Neurons were successfully segregated into three physiological clusters: regular-, intermediate-, and fast-spiking cells using cluster analysis as a multivariate exploratory technique. When morphological types of neurons were mapped on the physiological clusters, the cluster of regular spiking cells contained all pyramidal cells, whereas the intermediate- and fast-spiking clusters consisted exclusively of interneurons. The cluster of fast-spiking cells contained all of the chandelier cells and the majority of local, medium, and wide arbor (basket) interneurons. The cluster of intermediate spiking cells predominantly consisted of cells with the morphology of neurogliaform or vertically oriented (double-bouquet) interneurons. Thus a quantitative approach enabled us to demonstrate that intrinsic electrophysiological properties of neurons in the monkey prefrontal cortex define distinct cell types, which also display distinct morphologies.
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