Elsevier

Progress in Neurobiology

Volume 55, Issue 3, 27 June 1998, Pages 257-332
Progress in Neurobiology

Cortical pathways to the mammalian amygdala

https://doi.org/10.1016/S0301-0082(98)00003-3Get rights and content

Abstract

The amygdaloid nuclear complex is critical for producing appropriate emotional and behavioral responses to biologically relevant sensory stimuli. It constitutes an essential link between sensory and limbic areas of the cerebral cortex and subcortical brain regions, such as the hypothalamus, brainstem, and striatum, that are responsible for eliciting emotional and motivational responses.

This review summarizes the anatomy and physiology of the cortical pathways to the amygdala in the rat, cat and monkey. Although the basic anatomy of these systems in the cat and monkey was largely delineated in studies conducted during the 1970s and 1980s, detailed information regarding the cortico-amygdalar pathways in the rat was only obtained in the past several years. The purpose of this review is to describe the results of recent studies in the rat and to compare the organization of cortico-amygdalar projections in this species with that seen in the cat and monkey.

In all three species visual, auditory, and somatosensory information is transmitted to the amygdala by a series of modality-specific cortico-cortical pathways (“cascades”) that originate in the primary sensory cortices and flow toward higher order association areas. The cortical areas in the more distal portions of these cascades have stronger and more extensive projections to the amygdala than the more proximal areas.

In all three species olfactory and gustatory/visceral information has access to the amygdala at an earlier stage of cortical processing than visual, auditory and somatosensory information.

There are also important polysensory cortical inputs to the mammalian amygdala from the prefrontal and hippocampal regions. Whereas the overall organization of cortical pathways is basically similar in all mammalian species, there is anatomical evidence which suggests that there are important differences in the extent of convergence of cortical projections in the primate versus the nonprimate amygdala.

Section snippets

Introduction

His operation on Benson was directed toward a specific part of the brain, the limbic system. It was a very old part of the brain, in terms of evolution. . . . It controlled the most primitive behavior—anger and fear, lust and hunger, attack and withdrawal. Reptiles like crocodiles had little else to direct their behavior. Man, on the other hand, had a cerebral cortex.

But the cerebral cortex was a recent addition. . . . The cortex had grown up around the limbic brain, which remained . . . embedded deep inside the new cortex. That cortex, which could feel love, and worry about ethical conduct, and write poetry, had to make an uneasy peace with the crocodile brain at its core. Sometimes, as in the case of Benson, the peace broke down, and the crocodile brain took over intermittently. (Michael Crichton, The Terminal Man).

These musings about the relationship of the cerebral cortex to the limbic system are actually the thoughts of a fictional character, Dr. John Ellis, a neurosurgeon in Michael Crichton's novel entitled “Terminal Man” (Crichton, 1972). Ellis had surgically implanted a remotely controlled stimulating electrode in the amygdala of Harry Benson, a patient with temporal lobe epilepsy, in an attempt to control sporadic episodes of violent behavior. Crichton's idea for the novel was inspired by the

General considerations

The primate amygdala is located in the anteromedial part of the temporal lobe, where it lies ventromedial to the striatum and anterior to the ventral portion of the hippocampal formation (Fig. 1E). It has a similar position in nonprimates, such as the rat and cat, in which the temporal lobe is not as well developed (Fig. 2E, Fig. 3C). The amygdala in all mammals is anatomically complex (Koikegami, 1963; Price et al., 1987), consisting of numerous nuclei that often merge with their neighbors, as

Amygdalar projections to subcortical regions involved in behavior and emotion

An understanding of the significance of cortico-amygdalar projections requires a knowledge of the functional anatomy of the amygdala. As mentioned previously, stimulation of the amygdala in humans produces emotional responses that are often associated with complex experiential hallucinations. The most common emotional response elicited is fear, although rage, and occasionally pleasurable feelings, may also be produced. Stimulation and ablation studies in experimental animals have shown that the

Neuroanatomical methods

Since this review focuses on the connections of the amygdala as revealed by experimental tract tracing techniques, it is of interest to briefly review these methods. There are two major classes of tract tracing methods, anterograde and retrograde.

Projections from the olfactory bulb in primates

Anterograde tract tracing studies have shown that the macaque monkey amygdala receives projections from both the olfactory bulb and the primary olfactory cortex of the piriform lobe (Carmichael et al., 1994; Turner et al., 1978) (Fig. 5A). The primary olfactory cortex, which is defined as those cortical areas which receive direct projections from the olfactory bulb, is comprised of several regions that form a continuous zone in the vicinity of the lateral olfactory tract (LOT), the main

Anatomy of the parietal and insular lobes of primates

The primary somatosensory cortex (SI; area 3, 1, and 2) in the monkey brain, as in humans, is located posterior to, and within, the central sulcus (Fig. 1). The intraparietal sulcus of the posterior parietal region separates the superior parietal lobule (area 5) from the inferior parietal lobule (area 7). Ventral to SI and area 7 is the second somatosensory cortex (SII). It is located on the inner face of the parietal operculum on the upper bank of the lateral (sylvian) fissure (Fig. 7). SII is

Anatomy of the occipital and temporal lobes of primates

The primate occipital lobe consists of numerous retinotopically-organized visual cortical areas (Van Essen, 1985). The largest is V1, the primary visual area, which occupies the occipital pole and most of the medial and lateral aspects of the occipital lobe (Fig. 1 and Fig. 16). On the lateral surface of the hemisphere, V1 approaches the lunate and inferior occipital sulci, where it is replaced by area V2 (Fig. 16). Just anterior to V2 is area V3, which is largely concealed within the depths of

Anatomical and functional aspects of the hippocampal and rhinal cortices

Studies in primates have shown that long-term declarative memory (i.e., memory of facts and events) is critically dependent on a series of adjacent structures located in the inferomedial portion of the temporal lobe that comprise the medial temporal lobe memory system (MTLMS) (Squire and Zola-Morgan, 1991). These structures include the perirhinal cortex (PRC; located along the fundus and lateral bank of the rhinal sulcus), the entorhinal cortex (ERC; located medial to the rhinal sulcus), the

Prefrontal projections to the amygdala in primates

The frontal lobe of the monkey, like that of humans, is the portion of the cerebral cortex located anterior to the central sulcus (Fig. 1). The primary motor area (area 4) and premotor/supplementary motor area (area 6) are located between the central and arcuate sulci. The prefrontal cortex (PFC), which may be defined as the cortical projection field of the mediodorsal thalamic nucleus (Rose and Woolsey, 1948), consists of all frontal areas located anterior to the arcuate sulcus. Thus, the PFC

Summary and conclusions

Anatomical and physiological studies performed during the last 50 years have demonstrated that the amygdala is a unique subcortical structure which receives sensory information from the sensory cortices of all of the major sensory modalities. Olfactory and gustatory/visceral information has access to the amygdala at an earlier stage of cortical processing than visual, auditory and somatosensory information. Thus, olfactory inputs arise from the olfactory bulb and primary olfactory cortex

Acknowledgements

The author is grateful for the excellent assistance of Janice Burns in preparing the manuscript and Neda Ostermann in preparing the photomicrographs. I would also like to thank Drs. Martin Cassell (University of Iowa) and Joseph LeDoux (New York University) for their valuable comments on an earlier version of this manuscript. This work was supported by NIH Grant NS19733.

References (370)

  • D.P. Cain et al.

    Responses of amygdala single units to odors in the rat

    Exper. Neurol.

    (1972)
  • J. Carlsen et al.

    The basolateral amygdaloid complex as a cortical-like structure

    Brain Res.

    (1988)
  • M.D. Cassell et al.

    Ultrastructural evidence for an olfactory-autonomic pathway through the rat central amygdaloid nucleus

    Neurosci. Lett.

    (1991)
  • J. Coleman et al.

    Extrastriate projections from thalamus to posterior occipital-temporal cortex in the rat

    Brain Res.

    (1980)
  • W.M. Cowan et al.

    The autoradiographic demonstration of axonal connections in the central nervous system

    Brain Res.

    (1972)
  • M. Davis et al.

    Fear-potentiated startle: a neural and pharmacological analysis

    Behavioural Brain Research

    (1993)
  • M. Davis et al.

    Neurotransmission in the rat amygdala related to fear and anxiety

    Trends in Neurosci.

    (1994)
  • J. de Olmos et al.

    Mapping of collateral projections with the HRP method

    Neurosci. Lett.

    (1977)
  • P.A. Femano et al.

    The effects of stimulation of substantia innominata and sensory receiving areas of the forebrain upon the activity of neurons within the amygdala of the anesthetized cat

    Brain Res.

    (1983)
  • R.F. Fitzgerald et al.

    Neophobia and conditioned taste aversion deficits in the rat produced by undercutting temporal cortex

    Physiology and Behavior

    (1983)
  • R. Adolphs et al.

    Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala

    Nature

    (1994)
  • J.P. Aggleton

    A description of intra-amygdaloid connections in old world monkeys

    Exp. Brain Res.

    (1985)
  • J.P. Aggleton

    Description of the amygdalo-hippocampal interconnections in the macaque monkey

    Exp. Brain Res.

    (1986)
  • Aggleton, J. P. (1992) The functional effects of amygdala lesions in humans: a comparison with findings from monkeys....
  • Aggleton, J. P. and Mishkin, M. (1986) The amygdala: sensory gateway to the emotions. In: Emotion: Theory, Research and...
  • J.P. Aggleton et al.

    Syndrome produced by lesions of the amygdala in monkeys (Macaca mulatta)

    J. Comp. Physiol. Psychol.

    (1981)
  • M. Alden et al.

    Organization of the efferent projections from the pontine parabrachial area to the bed nucleus of the stria terminalis and neighboring regions: a PHA-L study in the rat

    J. Comp. Neurol.

    (1994)
  • Alheid, G. F., de Olmos, J. S. and Beltramino, C. A. (1995) Amygdala and extended amygdala. In: The Rat Nervous System,...
  • G.V. Allen et al.

    Organization of viseral and limbic connections of the insular cortex of the rat

    J. Comp. Neurol.

    (1991)
  • D.G. Amaral et al.

    Retrograde transport of D-[3H]-asparate injected into the monkey amygdaloid complex

    Exp. Brain Res.

    (1992)
  • Amaral, D. G., Price, J. L., Pitkanen, A. and Carmichael, S. T. (1992) Anatomical organization of the primate amygdala....
  • S.T. Azuma et al.

    Studies on gustatory responses of amygdaloid neurons in rats

    Exp. Brain Res.

    (1984)
  • J. Bancaud et al.

    Anatomical origin of dejá vu and vivid `memories' in human temporal lobe epilepsy

    Brain

    (1994)
  • E.M. Barnett et al.

    Anterograde tracing of trigeminal afferent pathways from the murine tooth pulp to cortex using herpes simplex virus type 1

    J. Neurosci.

    (1995)
  • G.C. Baylis et al.

    Functional subdivisions of the temporal lobe neocortex

    J. Neurosci.

    (1987)
  • R.M. Beckstead

    An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal-projection (prefrontal) cortex in the rat

    J. Comp. Neurol.

    (1979)
  • R.M. Beckstead et al.

    The nucleus of the solitary tract in the monkey: projections to the thalamus and brainstem nuclei

    J. Comp. Neurol.

    (1980)
  • F.M. Benes et al.

    Quantitative cytoarchitectural studies of the cerebral cortex in schizophrenics

    Arch. Gen. Psychiat.

    (1986)
  • J.F. Bernard et al.

    The organization of the efferent projections from the pontine parabrachial area to the amygdaloid complex: a Phaseolus vulgaris leucoagglutinin (PHA-L) study in the rat

    J. Comp. Neurol.

    (1993)
  • J.-F. Bernard et al.

    Convergence d'informations nociceptives sur des neurones parabrachio-amygdaliens chez le rat

    C. R. Acad. Sci. Paris

    (1988)
  • J.F. Bernard et al.

    Nucleus centralis of the amygdala and the globus pallidus ventralis: electrophysiological evidence for an involvement in pain processes

    J. of Neurophysiol.

    (1992)
  • E. Bonda et al.

    Specific involvement of human parietal systems and the amygdala in the perception of biological motion

    J. Neurosci.

    (1996)
  • F. Bordi et al.

    Sensory tuning beyond the sensory system: an initial analysis of auditory response properties of neurons in the lateral amygdaloid nucleus and overlying areas of the striatum

    J. Neuroscience

    (1992)
  • F. Bordi et al.

    Response properties of single units in areas of rat auditory thalamus that project to the amygdala

    Exp. Brain Res.

    (1994)
  • F. Bordi et al.

    Single-unit activity in the lateral nucleus of the amygdala and overlying areas of the striatum in freely behaving rats: rates, discharge patterns, and responses to acoustic stimuli

    Beh. Neurosci.

    (1993)
  • E.M. Bowman et al.

    Visual and auditory association areas of the cat's posterior ectosylvian gyrus: cortical afferents

    J. Comp. Neurol.

    (1988)
  • Brodman, K. (1909) Vergleichende Lokalisation Lehre der Grosshirnrinde in Ihren Prinzipien Dagestellt auf Grund des...
  • L.A. Brothers et al.

    Physiological evidence for an excitatory pathway from entorhinal cortex to amygdala in the rat

    Brain Res.

    (1985)
  • S. Brown et al.

    An investigation into the functions of the occipital and temporal lobes of the monkey"s brain

    Philos. Trans. R. Soc. Lond. [Biol]

    (1888)
  • Brown, T. H., Chang, V. C., Ganong, A. H., Keenan, C. L. and Kelso, S. R. (1988) Biophysical properties of dendrites...
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