Mapping of locomotor behavioral arousal induced by microinjections of dopamine within nucleus accumbens septi of rat forebrain

doi:10.1016/S0006-8993(97)00777-4

Brain Research

Volume 771, Issue 1, 10 October 1997, Pages 55-62

https://doi.org/10.1016/S0006-8993(97)00777-4 Get rights and content

Abstract

Dopamine (DA) at ca. ED₅₀ (16 μg) or saline was stereotaxically microinjected unilaterally 2 h after pretreatment with an MAO inhibitor into left or right nucleus accumbens septi of 697 freely moving rats (1394 injections) to define subregions involved in DA-induced behavioral arousal throughout the anatomical extent of the accumbens. Locomotion was quantified electronically and behavioral responses were assigned to histologically verified injection sites; postural or stereotyped behaviors characteristic of DA injections in caudate-putamen did not occur. Screening with 60 injections across mid-accumbens (2.2–3.2 mm rostral to bregma) indicated that locomotion was elicited non-homogeneously, and was particularly intense dorsomedially. Sites yielding intense arousal and their inactive surround were mapped along the rostrocaudal axis (1.4–4.2 mm anterior to bregma) in coronal sections. Responses to DA showed lateral symmetry and were similar across rostrocaudal levels, with intense responses in dorsomedial accumbens along its border with the caudate-putamen. This functional localization does not coincide closely with reported distributions of DA or its receptors, nor with histologically or histochemically defined core-shell regions of this limbic structure. Nucleus accumbens in rat brain thus appears to be organized functionally into distinct subregions differing markedly in ability to produce locomotor hyperactivity in response to exogenous DA.

Introduction

Dopamine (DA) containing neuronal systems in mammalian brain arise in midbrain and project to forebrain areas subserving movement-initiating functions and other aspects of behavioral arousal and reinforcement 4, 5, 7, 56. Deficient DA activity in the extrapyramidal basal ganglia is well known in Parkinson's disease and implicated in extrapyramidal side effects of DA antagonist neuroleptic drugs 4, 5. Abnormal mesolimbic or mesocortical DA function is also hypothesized in severe neuropsychiatric disorders marked by psychosis or mania, suggested in disorders of attention and the regulation of motor activity, and may be involved in the reinforcing or addictive properties of DA agonist stimulants and other drugs of abuse 4, 5, 6, 7, 41, 55, 58.

An important component of mammalian basal forebrain regions prominently innervated by DA is the nucleus accumbens septi (`accumbens') 43, 44. The anatomy of DA-containing neurons and afferent and efferent relationships within the rat accumbens have been explored extensively 30, 43, 44, 68. It shows many cytoarchitectural and histochemical similarities to its larger dorsal neighbor, the caudate-putamen complex (neostriatum), as well as some parallel fiber connections 14, 21, 48. Striatum receives afferent projections from anterior cerebral cortex and projects efferents through pallidum to thalamus which, in turn, completes a circuit back to the cortex 1, 28. Similarly, fibers from prefrontal or piriform cerebral cortex terminate in the ventral striatal-accumbens area 8, 22, 57, 63.

Accumbens is histologically and histochemically heterogeneous 32, 46, with two anatomically prominent subregions (a `core' and `shell') in rat brain, and perhaps in other species. These histological divisions are particularly distinct in mid-accumbens but less so at more rostral or caudal levels 27, 31. In rat accumbens, the core surrounds the rostral limb of the anterior commissure and contains a complex patch-matrix histological organization like the caudate-putamen; in mid-accumbens, the shell is medial, ventral and lateral in location. The shell, particularly caudally, has higher concentrations of DA, serotonin, substance P, acetylcholinesterase, and opioid receptors 20, 27, 28, 31, 32, 45, 46, 61, 62, 65, 67, 69, but the core is more sensitive to increases of DA synthesis by neuroleptics [20]and to neurotoxic effects of 6-hydroxydopamine [66]. The accumbens core projects primarily to dorsolateral pallidum, midbrain substantia nigra, ventrolateral mesencephalic tegmentum, and entopeduncular nucleus; the shell projects mainly to ventromedial pallidum and medial midbrain structures [31].

In contrast to a relatively abundant neuroanatomical analysis of rat accumbens, the distribution of behavioral or other functional effects of DA within this nucleus is less well defined. A role of accumbens in locomotion as an expression of behavioral arousal in response to DA or its agonists is well established, and can be elicited by unilateral as well as bilateral injections of DA 11, 12, 13, 17, 18, 24, 33, 52, 53, 60, 64. However, analyses of behavioral responses in subregions within accumbens are limited 11, 12, 13, 24, 60. The histological and histochemical heterogeneity of rat accumbens 32, 46suggests functional heterogeneity as well and led to the present experiments. Using previously detailed methods 11, 12, 13, we systematically examined regional variations in locomotion induced by local injection of a fixed dose of DA within the anatomically defined extent of rat nucleus accumbens. A guiding proposal was that the superimposition of large numbers of active and inactive responses would reveal patterns of regional variation that might not be shown reliably with a small number of even highly precise microinjections due to diffusion of DA into potentially large spheres of influence.

Section snippets

Animals and neurosurgical preparation

Animal procedures were approved by the Institutional Animal Care and Use Committee of McLean Hospital. A total of 697 young adult male, Sprague–Dawley albino rats (initial body weight 250–300 g) were first adapted for at least 1 week to a 12 h light-dark cycle (lights on 07.00–19.00 h) in a controlled environment (21–23°C, 40–50% humidity), with free access to standard food pellets and automatically delivered tap water. Subjects were anesthetized with sodium pentobarbital (60 mg/kg, i.p.) 15

Results

A total of 697 freely moving rats were given a ca. ED₅₀ dose of DA (16 μg, 0.105 μmol) unilaterally into the accumbens and a corresponding injection of saline as a vehicle control (total of 1394 injections and behavioral tests). Based on analysis of the time-course for 30 representative animals injected midway along the rostrocaudal extent of the accumbens (`mid-accumbens', 3.2 mm anterior to bregma), the onset of locomotor activity from DA-responsive sites at that level was virtually immediate

Discussion

Local injection of DA into the accumbens of unanesthetized, freely moving rats is known to stimulate locomotor activity 11, 12, 13, 17, 18, 24, 33, 52, 53, 60, 64, particularly following bilateral injections of DA into the dorsomedial region of mid-accumbens [16], consistent with the present findings (Fig. 1). Similarly, bilateral injection of D₂ or D₁ DA agonists into rat accumbens can also affect locomotor activity 24, 51, 59, 60. Conversely, bilateral destruction of accumbens DA neurons

Acknowledgements

Supported, in part, by USPHS (NIMH) Grants MH-31154 and MH-34006, RSA MH-47370, a grant from the Bruce J. Anderson Foundation, and awards from the Mailman Research Center Private Donors Neuropharmacology Research Fund (R.J.B.), and Training Grant MH-14275 (S.K.Y.).

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¹: Present address: Department of Neurosurgery, Duke University Medical Center, Durham, NC, USA.

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Research reportMapping of locomotor behavioral arousal induced by microinjections of dopamine within nucleus accumbens septi of rat forebrain

Abstract

Introduction

Section snippets

Animals and neurosurgical preparation

Results

Discussion

Acknowledgements

Neuroscience

Brain Res.

Brain Res. Rev.

Neurosci. Lett.

Neuroscience

Neuropharmacology

Brain Res.

Eur. J. Pharmacol.

Neurosci. Lett.

Eur. J. Pharmacol.

Brain Res.

Brain Res.

Neuroscience

Neuroscience

Neuroscience

Neuroscience

Mol. Brain Res.

Eur. J. Pharmacol.

Pharmacol. Biochem. Behav.

Behav. Brain Res.

Trends Neurosci.

Neuroscience

Prog. Brain Res.

Neuroscience

Brain Res.

Eur. J. Pharmacol.

Neurosci. Behav. Rev.

Behav. Brain Res.

Brain Res.

Brain Res.

Neuroscience

Parallel organization of functionally segregated circuits linking basal ganglia and cortex

Annu. Rev. Neurosci.

Brain dopamine receptors: a primer on their current status, basic and clinical

Harv. Rev. Psychiatry

Research report
Mapping of locomotor behavioral arousal induced by microinjections of dopamine within nucleus accumbens septi of rat forebrain