Amygdala input monosynaptically innervates parvalbumin immunoreactive local circuit neurons in rat medial prefrontal cortex

Gabbott, P.L.A.; Warner, Tracy; Busby, S.J.

doi:10.1016/j.neuroscience.2006.01.026

Cited by 111 publications

(99 citation statements)

References 61 publications

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“…Consistent with previous reports, these findings showed that the most prominent effect of BLA stimulation seems to be an evoked inhibition of mPFC neuron firing (Floresco and Tse, 2007;Pérez-Jaranay and Vives, 1991). The glutamatergic projections from the BLA that synapse onto PV-positive GABAergic interneurons provide one potential local feedforward inhibitory effect that can suppress firing of large groups of neurons (Gabbott et al, 1997(Gabbott et al, , 2006. In a similar manner, afferent input of the hippocampus to the mPFC contacts both pyramidal neurons and inhibitory GABAergic interneurons (Gabbott et al, 2002).…”

Section: Modulatory Influence Of Bla On Vhipp-evoked Firing In Mpfc Isupporting

confidence: 91%

“…In contrast to the BLA input, we did not observe any inhibitory effect of the vHipp input on BLA-evoked firing in mPFC in controls. These findings suggest that the facilitation of hippocampal-evoked firing after stimulation of the BLA afferents preferentially activates feedforward excitatory circuits, provided by glutamatergic synapses on spines of the prefrontal pyramidal neurons (Gabbott et al, 2006). In contrast, the BLA projection seems to preferentially activate mPFC fast-spiking interneurons at shorter latencies compared with the pyramidal neurons.…”

Section: Modulatory Influence Of Bla On Vhipp-evoked Firing In Mpfc Imentioning

confidence: 80%

“…In contrast to the effects of BLA stimulation on vHipp-mPFC-evoked responses, there was no inhibitory period when examining the effects of vHipp stimulation on BLA-mPFC-evoked responses in control rats. Pyramidal neurons and PV-immunoreactive GABAergic interneurons in different subregions of the mPFC, including the prelimbic and infralimbic cortices, receive glutamatergic projections from the BLA (Gabbott et al, 2006;McDonald, 1991;Mcdonald, 1996;Shinonaga et al, 1994). Previous electrophysiological recordings reported that BLA inputs exerted both inhibition and excitation of mPFC neurons.…”

Section: Modulatory Influence Of Bla On Vhipp-evoked Firing In Mpfc Imentioning

confidence: 99%

“…Together, these systems have a role in the regulation of fear memory, reward associated learning, drug addiction, and anxiety disorders. In the rat, the vHipp has glutamatergic projections to both pyramidal neurons and GABAergic interneurons of the prelimbic region of the mPFC (Carr and Sesack, 1996;Gabbott et al, 2002Gabbott et al, , 2006. Stimulation of the hippocampus is known to evoke excitatory and inhibitory responses in mPFC neurons (Gigg et al, 1994;Jay et al, 1995).…”

Section: Introductionmentioning

confidence: 99%

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Afferent Drive of Medial Prefrontal Cortex by Hippocampus and Amygdala is Altered in MAM-Treated Rats: Evidence for Interneuron Dysfunction

Esmaeili

Grace

2013

Neuropsychopharmacol

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Evidence indicates that the prefrontal cortex and its regulation by afferent inputs are disrupted in schizophrenia. Using a validated rat model of schizophrenia based on prenatal administration of the mitotoxin methyl azoxymethanol acetate (MAM), we examined the convergent projections from the ventral hippocampus (vHipp) and the basolateral amygdala (BLA) in the medial prefrontal cortex (mPFC). In vivo extracellular recordings were done in anesthetized rats to assess how prior stimulation of the BLA or vHipp input to the mPFC affected mPFC responses to subsequent stimulation of these regions. The interstimulus interval (ISI) of the BLA and vHipp pulse stimulation was varied randomly between 0 and 130 ms, and the probability of evoked spike response in the mPFC measured. We found that BLA input increased vHipp-evoked spike probability at ISIs 40-130 ms, but decreased spike probability at ISIs 10-20 ms. This would be consistent with activation of inhibitory interneurons at shorter ISIs by BLA stimulation. In contrast, in MAM-treated rats BLA stimulation increased vHipp-evoked spike probability in mPFC at all ISIs tested. Given that interneurons are driven primarily by N-methyl-D-aspartate (NMDA) channel activation, the effects of the NMDA channel blocker, phencyclidine (PCP), were tested. PCP was found to completely attenuate the inhibitory effect of BLA input on vHipp-evoked responses in mPFC at shorter ISIs, causing the response in control rats treated with PCP to resemble that observed in the MAM rat. In contrast to the effects of BLA stimulation on vHipp-mPFCevoked responses, there was no inhibitory period when examining the effects of vHipp stimulation on BLA-mPFC-evoked responses in control rats, but in MAM-treated rats there was a significant inhibition at short intervals. Thus, both affective input arising from the BLA and context-dependent input from the vHipp exert a modulatory effect on mPFC neural activity in response to these inputs. Whereas the BLA potentiated vHipp input to the mPFC at long intervals, there was a short-interval inhibitory period that appeared to be mediated by an NMDA-dependent drive of interneurons. This inhibitory modulation was absent in the model of schizophrenia and following PCP, which is consistent with an interneuron disruption in this disorder.

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Section: Modulatory Influence Of Bla On Vhipp-evoked Firing In Mpfc Isupporting

confidence: 91%

Section: Modulatory Influence Of Bla On Vhipp-evoked Firing In Mpfc Imentioning

confidence: 80%

Section: Modulatory Influence Of Bla On Vhipp-evoked Firing In Mpfc Imentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Afferent Drive of Medial Prefrontal Cortex by Hippocampus and Amygdala is Altered in MAM-Treated Rats: Evidence for Interneuron Dysfunction

Esmaeili

Grace

2013

Neuropsychopharmacol

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“…This means that PV+ cell activation can contribute to the silencing of pyramidal neuron activity in a layer-specific manner (Gonzalez-Islas and Hablitz, 2001;Gulledge and Jaffe, 2001;Seamans et al, 2001;Tseng and O'Donnell, 2004;. Following drug administration, there are data to implicate GABA transmission in the motor stimulant response (Karler et al, 1997;Bartoletti et al, 2005); however, no studies differentiate the regional or lamina-specific effects of inhibitory interneurons.Dopaminergic terminals from VTA neurons form dense contacts onto interneurons in layers V and VI (Sesack et al, 1995) and excitatory afferents from limbic and thalamic regions innervate specific layers where they contact both PV+ interneurons and pyramidal cells (Gabbott et al, 2002;Rotaru et al, 2005;Gabbott et al, 2006). Since layer III pyramidal neurons connect the mPFC to other cortices, and layer V and VI pyramidal cells project primarily to subcortical targets (Jones, 1984;Gabbott et al, 2005), PV+ interneurons are ideally positioned to shape the receptive fields of pyramidal cells in a layer-specific manner.…”

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confidence: 99%

Differential laminar effects of amphetamine on prefrontal parvalbumin interneurons

Morshedi

Meredith

2007

Neuroscience

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The increase in excitatory outflow from the medial prefrontal cortex is critical to the development of sensitization to amphetamine. There is evidence that psychostimulant-induced changes in dopamine-GABA interactions are key to understanding the behaviorally sensitized response. The objective of this study was to characterize the effects of different amphetamine paradigms on the Fos activation of GABAergic interneurons that contain parvalbumin in the medial prefrontal cortex. Although a sensitizing, repeated regimen of amphetamine induced Fos in all cortical layers, only layer V parvalbumin-immunolabeled cells were activated in the infralimbic and prelimbic cortices. Repeated amphetamine treatment was also associated with a loss of parvalbumin immunoreactivity in layer V, but only in the prelimbic cortex. An acute amphetamine injection to naïve rats was associated with an increase in Fos, but in parvalbumin-positive neurons of the prelimbic cortex, where it was preferentially induced in layer III. These data indicate that distinct substrates mediate the response to repeated or acute amphetamine treatment. They also suggest that a sensitizing amphetamine regimen directs mPFC outflow, via changes in inhibitory neuron activation, towards subcortical centers important in reward.Keywords prelimbic cortex; infralimbic cortex; GABA; dopamine; Fos; behavioral sensitization Repeated amphetamine (AMPH) exposure in humans has been associated with long-lasting changes in behavior (Robinson and Berridge, 2000). In experimental animals, such treatment progressively augments locomotion (behavioral sensitization), an effect that persists after treatment and can be measured by a drug challenge (Wolf, 1998). Sensitization to AMPH appears to require changes in dopamine and excitatory amino acid transmission in the medial prefrontal cortex (mPFC) and ventral tegmental area (VTA) (Wolf et al., 1995;Li and Wolf, 1997;Tzschentke and Schmidt, 2000;Wolf et al., 2003). Lesions of the mPFC block the development of sensitization, whether AMPH is repeatedly injected systemically or intra-VTA (Wolf et al., 1995;Li and Wolf, 1997;Cador et al., 1999; but see Tzschentke and Schmidt, 2000). AMPH sensitization also induces region-specific increases in mPFC Fos expression (Hedou et al., 2002), although the active neurons have yet to be fully identifed.Correspondence should be addressed to Maud M. Morshedi, Department of Cellular and Molecular Pharmacology, Chicago Medical School, Rosalind Franklin University of Medicine and Science, 3333 Green Bay Road, North Chicago, IL 60064, USA, (maud.morshedi@students.rosalindfranklin.edu). Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could ...

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Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat

Vertes

Hoover

2008

J of Comparative Neurology

253

265

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The paraventricular (PV) and paratenial (PT) nuclei are prominent cell groups of the midline thalamus. To our knowledge, only a single early report has examined PV projections and no previous study has comprehensively analyzed PT projections. By using the anterograde anatomical tracer, Phaseolus vulgaris leucoagglutinin, and the retrograde tracer, FluoroGold, we examined the efferent projections of PV and PT. We showed that the output of PV is virtually directed to a discrete set of limbic forebrain structures, including 'limbic' regions of the cortex. These include the infralimbic, prelimbic, dorsal agranular insular, and entorhinal cortices, the ventral subiculum of the hippocampus, dorsal tenia tecta, claustrum, lateral septum, dorsal striatum, nucleus accumbens (core and shell), olfactory tubercle, bed nucleus of stria terminalis (BST), medial, central, cortical, and basal nuclei of amygdala, and the suprachiasmatic, arcuate, and dorsomedial nuclei of the hypothalamus. The posterior PV distributes more heavily than the anterior PV to the dorsal striatum and to the central and basal nuclei of amygdala. PT projections significantly overlap with those of PV, with some important differences. PT distributes less heavily than PV to BST and to the amygdala, but much more densely to the medial prefrontal and entorhinal cortices and to the ventral subiculum of hippocampus. As described herein, PV/PT receive a vast array of afferents from the brainstem, hypothalamus, and limbic forebrain, related to arousal and attentive states of the animal, and would appear to channel that information to structures of the limbic forebrain in the selection of appropriate responses to changing environmental conditions. Depending on the specific complement of emotionally associated information reaching PV/PT at any one time, PV/PT would appear positioned, by actions on the limbic forebrain, to direct behavior toward a particular outcome over a range of outcomes.

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Amygdala input monosynaptically innervates parvalbumin immunoreactive local circuit neurons in rat medial prefrontal cortex

Cited by 111 publications

References 61 publications

Afferent Drive of Medial Prefrontal Cortex by Hippocampus and Amygdala is Altered in MAM-Treated Rats: Evidence for Interneuron Dysfunction

Afferent Drive of Medial Prefrontal Cortex by Hippocampus and Amygdala is Altered in MAM-Treated Rats: Evidence for Interneuron Dysfunction

Differential laminar effects of amphetamine on prefrontal parvalbumin interneurons

Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat

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