Elsevier

Neuroscience

Volume 77, Issue 2, 21 February 1997, Pages 445-459
Neuroscience

Projections of the lateral entorhinal cortex to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat

https://doi.org/10.1016/S0306-4522(96)00478-2Get rights and content

Abstract

In addition to providing a gateway to the hippocampus, the entorhinal cortex has significant projections to the amygdala. In the present investigation, the organization of the projections of the lateral entorhinal cortex to the amygdala was studied in the rat using the sensitive anterograde tracer Phaseolus vulgaris leucoagglutinin. Each of the three main subdivisions of the lateral entorhinal cortex provided a characteristic projection to the amygdala that mainly arose from the deep cortical layers. The projections from the dorsolateral and ventrolateral entorhinal areas were much stronger than those arising from the ventromedial entorhinal area. The primary targets of the dorsolateral and ventrolateral entorhinal areas were the basolateral amygdala, lateral capsular subdivision of the central nucleus and caudal portions of the cortical nuclear complex. The dorsolateral entorhinal area projects mainly to the lateral part of the basal nucleus, while the ventrolateral entorhinal area projects mainly to its medial part. A transitional region at the rostral pole of the ventrolateral entorhinal cortex has additional strong projections to the lateral subdivision of the central nucleus, medial amygdaloid nucleus and the intra-amygdaloid portion of the bed nucleus of the stria terminalis.

The results of the present study indicate that the amygdala is one of the principal targets of the entorhinal cortex. The correspondence between the topography of entorhino-hippocampal connections and entorhino-amygdaloid connections suggests that the amygdaloid projection arising in each of the three main subdivisions of the entorhinal cortex conveys information processed in different septotemporal portions of the hippocampal formation. These entorhinal projections, which probably convey complex relational (including contextual) information to the amygdala, are in a position to produce different behavioral responses by activating different portions of the amygdaloid nuclear complex.

Section snippets

Experimental procedures

A total of 26 adult, male Sprague–Dawley rats (Harlan) received stereotaxic injections of PHA-L (2.5% PHA-L dissolved in 10 mM phosphate buffer, pH 8.0) into the entorhinal cortex. Stereotaxic coordinates were obtained from an atlas of the rat brain.[43]Animals were anesthetized with sodium pentobarbital (50 mg/kg). Injections were made iontophoretically using a Midgard high-voltage current source set at 5.0 μA (7 s on, 7 s off for 30–45 min). Micropipettes had an inner tip diameter of 25 μm. After a

Results

Fig. 1 illustrates the location of PHA-L injection sites in the entorhinal cortex in different cases. Twenty-one animals received injections that were confined to one of the three subdivisions of the LEA (DL: n=10; VL: n=8; VM: n=3). One animal (case E-59) had an injection at the junction of the DL and VL at rostral entorhinal levels (Fig. 1B). Four animals had injections at the border separating the dorsolateral and medial entorhinal areas (Fig. 1H).

Each of the three subdivisions of the LEA

Discussion

The present investigation is the first detailed anterograde study of lateral entorhinal projections to the rat amygdala. The results indicate that the amygdala is one of the major targets of lateral entorhinal efferents. The projections to the amygdala arise primarily from the deep layers of the entorhinal cortex and exhibit a topographical organization. The projection arising from the DL and VL is much stronger than that originating from the VM. The main targets of the DL and VL are the

Conclusions

The projection of the entorhinal cortex to the amygdala in the rat is both robust and extensive. It originates primarily from the deep layers of the cortex and is topographically organized. The projections of the DL and VL are much stronger than the projections arising from the VM. The main target of the DL is the lateral part of the basolateral amygdala, whereas the VL mainly targets medial portions of this complex. Projections are also seen to the CLC and cortical nuclei. Additional

Acknowledgements

This work was supported by National Institutes of Health Grant NS19733. The authors are grateful for the technical assistance of Yvonne Riley, the secretarial support of Janice Burns and the photographic assistance of Neda Osterman.

References (61)

  • J.G Veening

    Cortical afferents of the amygdaloid complex in the rat: an HRP study

    Neurosci. Lett.

    (1978)
  • M.P Witter et al.

    Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region

    Prog. Neurobiol.

    (1989)
  • Aggleton J. P. and Mishkin M. (1986) The amygdala: sensory gateway to the emotions. In Emotion: Theory, Research and...
  • Amaral D. G., Price J. L., Pitkanen A. and Carmichael S. T. (1992) Anatomical organization of the primate amygdala. In...
  • Amaral D. G. and Witter M. P. (1995) Hippocampal formation. In The Rat Nervous System (ed. Paxinos G.), pp. 443–494....
  • R.M Beckstead

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

    J. comp. Neurol.

    (1979)
  • L.A Brothers et al.

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

    Brain Res.

    (1985)
  • N.S Canteras et al.

    Connections of the posterior nucleus of the amygdala

    J. comp. Neurol.

    (1992)
  • N.S Canteras et al.

    Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat

    J. comp. Neurol.

    (1992)
  • Davis M. (1992) The role of the amygdala in conditioned fear. In The Amygdala: Neurobiological Aspects of Emotion,...
  • T.V Deacon et al.

    Afferent connections of the perirhinal cortex in the rat

    J. comp. Neurol.

    (1983)
  • H Eichenbaum et al.

    Two functional components of the hippocampal memory system

    Behav. Brain Sci.

    (1994)
  • M.S Fanselow et al.

    Acquisition of contexual Pavlovian fear conditioning is blocked by application of an NMDA receptor antagonist d,l-2-amino-5-phosphonovaleric acid to the basolateral amygdala

    Behav. Neurosci.

    (1994)
  • Gaffan D. (1992) Amygdala and the memory of reward. In The Amygdala: Neurobiological Aspects of Emotion, Memory, and...
  • C.R Gerfen et al.

    An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L) tract tracing and immunohistochemistry

    Brain Res.

    (1984)
  • Gloor P. (1972) Temporal lobe epilepsy: its possible contribution to the understanding of the functional significance...
  • H.J Groenewegen et al.

    The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization

    Prog. Brain Res.

    (1990)
  • Hall E. (1972) Some aspects of the structural organization of the amygdala. In The Neurobiology of the Amygdala (ed....
  • M.B Hancock

    Two color immunoperoxidase staining: visualization of anatomic relationships between immunoreactive neural elements

    Am. J. Anat.

    (1986)
  • R Insausti et al.

    The entorhinal cortex of the monkey: II. Cortical afferents

    J. comp. Neurol.

    (1987)
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