Elsevier

Brain Research Reviews

Volume 24, Issues 2–3, 19 September 1997, Pages 197-254
Brain Research Reviews

Full-length review
The structural organization of connections between hypothalamus and cerebral cortex1

https://doi.org/10.1016/S0165-0173(97)00007-6Get rights and content

Abstract

Motivated behavior requires coordinated somatic, autonomic, and endocrine responses, and may be divided into initiation, procurement, and consummatory phases (Swanson, L.W. and Mogenson, G.J., Neural mechanisms for the functional coupling of autonomic, endocrine and somatomotor responses in adaptative behavior, Brain Res. Rev., 3 (1981) 1–34). Obviously, such behavior may involve the entire central nervous system, although it is important to identify circuitry or systems that mediate the behavior directed toward specific goal objects. This problem has recently been clarified by the identification of hypothalamic subsystems important for the execution of instinctive behaviors related to ingestion, reproduction, and defense. These subsystems are modulated by sensory (reflex), central control (e.g., circadian), and voluntary (cortical) inputs. The latter are dominated by inputs from the ventral temporal lobe and medial prefrontal region, which are both direct and via associated parts of the basal nuclei (ganglia). Hypothalamic output is characterized by descending projections to brainstem and spinal motor systems, and by projections back to the cerebral cortex, which are both direct and via a continuous rostromedial part of the dorsal thalamus. This thalamic region includes the anterior, medial, and midline groups, which in turn innervate a continuous ring of cortex that includes the hippocampal formation and the cingulate, prefrontal, and insular regions. Parts of this thalamic region also innervate the ventral striatum, which receives a massive input from the cortical ring as well.

Introduction

The hypothalamus is a relatively small division of the vertebrate forebrain that plays an especially important role in neural mechanisms assuring homeostasis, defense, and reproduction — that is, in assuring survival of the animal as well as the species. The most convincing evidence for this view is based on the results of ablation and lesion studies, supplemented by experiments utilizing electrical or chemical stimulation within specific parts of the hypothalamus 52, 113, 187, 215. Broadly speaking, the physiological work to date suggests a model wherein: (a) the hypothalamus coordinates the somatic, autonomic, and neuroendocrine motor responses typical of the various classes of motivated (goal-oriented) behavior; (b) foraging or exploratory behavior associated with specific goal objects is initiated and directed by the telencephalon; and (c) motor responses themselves are initiated from the brainstem (including the hypothalamus itself) and spinal cord as a whole 272, 284. Put another way, the hypothalamus may contain neural substrates for coordinating the various instinctive behaviors necessary for survival, behaviors that can be initiated either directly by sensory inputs (reflex activation) or indirectly by cerebral cortical inputs (voluntary activation).

Structural information about the organization of neural systems that mediate homeostasis and goal-oriented behavior has accumulated more slowly than functional information. The purpose of this review, which is based on the literature as well as on original observations that fill major gaps in the literature, is to provide an overview of what is currently known about one important aspect of this problem: the organization of connections between the hypothalamus and cerebral cortex. Views about corticohypothalamic relationships have changed considerably since axonal tracer and immunohistochemical methods became widely used in the 1970s. From an incisive review of the earlier literature Nauta and Haymaker concluded in 1969 [191]that four telencephalic regions, the prefrontal cortex, hippocampus, amygdala, and olfactory cortex project directly to the hypothalamus, and that the hypothalamus projects back to essentially the same regions (by way of direct lateral hypothalamic to amygdala projections; lateral preoptic/lateral hypothalamic to mediodorsal thalamus to prefrontal cortical projections; mammillary to anterior thalamus to cingulate gyrus projections; and lateral hypothalamic to septum to hippocampus projections).

Much more is now known about four major routes from the hypothalamus to the cerebral cortex (Fig. 1). They include a massive, direct projection to all parts of the cortical mantle, and three indirect routes by way of the thalamus, endbrain basal nuclei (ganglia), and brainstem. The organization of these pathways will be reviewed, along with what is known about projections from the cerebral cortex to the hypothalamus. However, special attention will be devoted to the organization of projections from the hypothalamus to the thalamus, which are more extensive than previously appreciated. And to make the results as functionally relevant as possible, the review will begin with a consideration of sensory inputs to intrahypothalamic subsystems defined by recent anatomical and functional work. The topographical relationship between these subsystems and the various functional regions of the cerebral cortex provides the basic framework for this review, which will concentrate on what is known in the rat where our neuroanatomical information is by far the most extensive. Section 2, Section 3, and Section 4will stress what is currently understood about the structural organization of pathways interrelating the hypothalamus and cerebral cortex, whereas the possible functional significance of this circuitry will be dealt with in Section 5. Unless otherwise indicated, the nomenclature used is from our atlas of the adult rat brain [274].

Section snippets

Sensory inputs to hypothalamic subsystems

To understand the organization of any neural system it is useful to begin with a consideration of sensory inputs, which are relatively easy to appreciate in functional terms. To place the current topic in perspective, it is interesting that Nauta and Haymaker [191]could not point to a single morphologically well-defined sensory input to the hypothalamus in 1969. The situation has changed dramatically in the last 25 years, and the relevant information has greatly clarified the functional

Hypothalamocortical pathways

We have just seen that a number of hypothalamic subsystems have now been identified, and provisionally associated with larger neural systems subserving different classes of motivated behavior, or visceral responses. These intrahypothalamic subsystems, as well as other hypothalamic areas not yet assigned to particular systems, receive sensory inputs. However, unlike the thalamus, which relays sensory information directly to the cerebral cortex, the hypothalamus is not usually thought to be

Corticohypothalamic pathways

This section provides a brief overview of telencephalic inputs to the hypothalamus — that is, direct projections from the cortical mantle, as well as projections from the basal nuclei that are presumably driven by inputs from the cortex.

Functional considerations

The cerebral cortex and hypothalamus share massive bidirectional connections. What is the functional role of the hypothalamus, and how is it modified by the cerebral cortex? In the following discussion, we shall attempt to clarify this problem by considering some of the organizing principles of forebrain circuitry suggested by the mass of anatomical information that has accumulated in the last 25 years and that was reviewed in the preceding sections. However, it needs to be emphasized that this

Abbreviations

AAAanterior amygdaloid area
acanterior commissure
ACAanterior cingulate area
ACAdanterior cingulate area, dorsal part
ACAvanterior cingulate area, ventral part
ACBnucleus accumbens
acoanterior commissure, olfactory limb
ADanterodorsal nucleus thalamus
ADPanterodorsal preoptic nucleus
AHAanterior hypothalamic area
AHNanterior hypothalamic nucleus
AHNaanterior hypothalamic nucleus, anterior part
AHNcanterior hypothalamic nucleus, central part
AHNdanterior hypothalamic nucleus, dorsal part
AHNpanterior

Acknowledgements

This work was supported in part by National Institutes of Health Grant NS16686.

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