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Glutamatergic input from specific sources influences the nucleus accumbens-ventral pallidum information flow

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Abstract

The nucleus accumbens (NAc) is positioned to integrate signals originating from limbic and cortical areas and to modulate reward-related motor output of various goal-directed behaviours. The major target of the NAc GABAergic output neurons is the ventral pallidum (VP). VP is part of the reward circuit and controls the ascending mesolimbic dopamine system, as well as the motor output structures and the brainstem. The excitatory inputs governing this system converge in the NAc from the prefrontal cortex (PFC), ventral hippocampus (vHC), midline and intralaminar thalamus (TH) and basolateral nucleus of the amygdala (BLA). It is unclear which if any of these afferents innervate the medium spiny neurons of the NAc, that project to the VP. To identify the source of glutamatergic afferents that innervate neurons projecting to the VP, a dual-labelling method was used: Phaseolus vulgaris leucoagglutinin for anterograde and EGFP-encoded adenovirus for retrograde tract-tracing. Within the NAc, anterogradely labelled BLA terminals formed asymmetric synapses on dendritic spines that belonged to medium spiny neurons retrogradely labelled from the VP. TH terminals also formed synapses on dendritic spines of NAc neurons projecting to the VP. However, dendrites and dendritic spines retrogradely labelled from VP received no direct synaptic contacts from afferents originating from mPFC and vHC in the present material, despite the large number of fibres labelled by the anterograde tracer injections. These findings represent the first experimental evidence for a selective glutamatergic innervation of NAc neurons projecting to the VP. The glutamatergic inputs of different origin (i.e. mPFC, vHC, BLA, TH) to the NAc might thus convey different types of reward-related information during goal-directed behaviour, and thereby contribute to the complex regulation of nucleus accumbens functions.

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Abbreviations

NAc:

Nucleus accumbens

mPFC:

Medial prefrontal cortex

vHC:

Ventral hippocampus

BLA:

Basolateral amygdala

PVT:

Paraventricular thalamic nucleus

VP:

Ventral pallidum

VTA:

Ventral tegmental area

PB:

Phosphate buffer

TBS:

Tris-buffered saline

PHAL :

Phaseolus vulgaris leucoagglutinin

EGFP:

Enhanced green fluorescent protein AdSynEGFP adenovirus vector using a neuron-specific synapsin I Promoter and enhanced green fluorescent protein reporter (EGFP)

vGluT2:

Vesicular glutamate transporter 2 (also known DNPI, Slc17a6)

TH:

Midline and intralaminar thalamus

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Acknowledgments

This work was supported by a NIH NS030549, NIH DA09158, EU GENADDICT LSHM-CT-2004-005166, NKTH-OTKA, CNK77793, HHMI 55005608 grants. The excellent technical assistance of E. Simon Szépné and Gy. Goda is also acknowledged. E. P. is a grantee of the János Bólyai scholarship.

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Authors and Affiliations

  1. Laboratory of Cerebral Cortex Research, Institute of Experimental Medicine, Hungarian Academy of Sciences, H-1450 Budapest, P.O. Box 67, Budapest, Hungary

    Edit Papp, Zsolt Borhegyi & Tamás F. Freund

  2. Center for Brain Research, Medical University of Vienna, Vienna, Austria

    Zsolt Borhegyi & Ryohei Tomioka

  3. Picower Inst. Learning and Memory, RIKEN-MIT Center for Neural Circuit Genetics, MIT, Cambridge, MA, 02139, USA

    Kathleen S. Rockland

  4. Department of Neurology and Physiology, The David Geffen School of Medicine, University of California, Los Angeles, CA, 90095, USA

    István Mody

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  1. Edit Papp
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  2. Zsolt Borhegyi
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Correspondence to Edit Papp.

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Papp, E., Borhegyi, Z., Tomioka, R. et al. Glutamatergic input from specific sources influences the nucleus accumbens-ventral pallidum information flow. Brain Struct Funct 217, 37–48 (2012). https://doi.org/10.1007/s00429-011-0331-z

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