Intra-amygdaloid projections of the basolateral and basomedial nuclei in the cat: Phaseolus vulgaris-leucoagglutinin anterograde tracing at the light and electron microscopic level

doi:10.1016/0306-4522(95)00272-K

Neuroscience

Volume 69, Issue 2, November 1995, Pages 567-583

https://doi.org/10.1016/0306-4522(95)00272-K Get rights and content

Abstract

The amygdaloid complex plays an essential role in auditory fear conditioning of the Pavlovian type. The available evidence suggests that the lateral nucleus is the input station of the amygdala for auditory conditioned stimuli, whereas the central medial nucleus is the output for conditioned fear responses. However, the intrinsic pathway transmitting auditory information about the conditioned stimulus from the lateral to the central medial nuclei is unknown as there are no direct projections between these nuclei. The present study was undertaken to determine if the main intra-amygdaloid targets of the lateral nucleus, namely the basomedial and basolateral nuclei, project to the central medial nucleus. To this end, iontophoretic injections of the anterograde tracer Paseolus vulgaris-leucoagglutinin were performed in these nuclei. To rule out the possibility that the anterograde labeling reflected passing fibers merging with the major fiber bundles that course in and around the central medial nucleus, labeled terminals and varicosities were observed in the electron microscope.

It was determined that the basolateral and basomedial nuclei have partially overlapping intraamygdaloid targets. They both project to the central medial nucleus, nucleus of the lateral olfactory tract and peri-amygdaloid cortex, but have limited projections to each other. Small Phaseolus vulgaris-leucoagglutinin injections in both nuclei gave rise to prominent intranuclear projections but only the basomedial nucleus was found to project to the lateral and anterior cortical nuclei. At the electron microscopic level, all labeled axon terminals and varicosities formed asymmetric synapses (n = 245) with dendritic spines (83%) or with dendritic shafts (17%).

This is the first unambiguous demonstration that the basolateral and basomedial nuclei project to the central medial nucleus. Since these nuclei constitute the main intra-amygdaloid targets of the lateral nucleus, they represent likely candidates for the transmission of auditory conditioned stimuli to the central medial nucleus in auditory fear conditioning.

References (55)

AndersenP.
Synaptic integration in hippocampal CA1 pyramids
CarlsenJ. et al.
The basolateral amygdaloid complex as a cortical-like structure
Brain Res.
(1988)
CaullerL.J. et al.
Functions of very distal dendrites: experimental and computational studies of layer I synapses on neocortical pyramidal cells
DeFelipeJ. et al.
The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs
Prog. Neurobiol.
(1992)
FarbC. et al.
Glutamate-immunoreactive terminals in the lateral amygdaloid nucleus
Brain Res.
(1992)
FrancisJ. et al.
Lateral hypothalamic lesions: effects on Pavlovian cardiac and eyeblink conditioning in the rabbit
Brain Res. Bull.
(1981)
GerfenC.R. et al.
An anterograde neuroanatomical tracing that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris-leucoagglutinin (PHA-L)
Brain Res.
(1984)
HolstegeG.
Subcortical limbic system projections to caudal brainstem and spinal cord
IwataJ. et al.
Intrinsic neurons in the amygdaloid field projected to by the medial geniculate body mediate emotional responses conditioned to acoustic stimuli
Brain Res.
(1986)
KappB.S. et al.
Amygdala central nucleus lesions: effects on heart rate conditioning in the rabbit
Physiol. Behav.
(1979)

LeDouxJ.E. et al.

Interruption of projections from the medial geniculate body to an archi-neostriatal field disrupts the classical conditioning of emotional responses to acoustic stimuli

Neuroscience

(1986)

McDonaldA.J.

Projection neurons of the basolateral amygdala: a correlative Golgi and retrograde tract tracing study

Brain Res. Bull.

(1992)

McDonaldA.J. et al.

Localization of GABA-like immunoreactivity in the monkey amygdala

Neuroscience

(1993)

ParéD. et al.

Distribution of GABA immunoreactivity in the amygdaloid complex of the cat

Neuroscience

(1993)

RusschenF.T. et al.

Amygdalostriatal projections in the rat. Topographical organization and fiber morphology shown using the lectin PHA-L as an anterograde tracer

Neurosci. Lett.

(1984)

VeeningJ.G. et al.

The organization of projections from the central nucleus of the amygdala to brainstem sites involved in central autonomic regulation: a combined retrograde transport-immunohistochemical study

Brain Res.

(1984)

WakefieldC.

The intrinsic connections of the basolateral amygdaloid nuclei as visualized with the HRP method

Neurosci. Lett.

(1979)

AggletonJ.P.

A description of intra-amygdaloid connections in old world monkeys

Expl Brain Res.

(1985)

AmaralD.G. et al.

Anatomical organization of the primate amygdaloid complex

BerkelyK.J.

Spatial relationships between the terminations of somatic sensory and motor pathways in the rostral brainstem of cats and monkeys. I. Ascending somatic sensory inputs to lateral diencephalon

J. comp. Neurol.

(1980)

CarlsenJ.

Immunocytochemical localization of glutamate decarboxylase in the rat basolateral amygdaloid nucleus, with special reference to GABAergic innervation of amygdalostriatal projection neurons

J. comp. Neurol.

(1988)

CaullerL.J. et al.

Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex

J. Neurosci.

(1994)

ColonnierM.

The electron-microscopic analysis of the neuronal organization of the cerebral cortex

GentileC.G. et al.

The role of amygdaloid central nucleus in differential Pavlovian conditioning of bradycardia in rabbits

Behav. Brain Res.

(1986)

HallE.

The amygdala of the cat: a Golgi study

Z. Zellforsch.

(1972)

HitchcockJ.M. et al.

Sensitization of the startle reflex by footshock: blockade by lesions of the central nucleus of the amygdala or its efferent pathway to the brainstem

Behav. Neurosci.

(1989)

HopkinsD.A. et al.

Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat

Expl Brain Res.

(1978)

Cited by (134)

Presynaptic HCN channel activity is required for the expression of long-term potentiation at lateral amygdala to basal amygdala synapses
2022, Biochemical and Biophysical Research Communications
Recently, we reported that auditory fear conditioning leads to the presynaptic potentiation at lateral amygdala to basal amygdala (LA-BA) synapses that shares the mechanism with high-frequency stimulation (HFS)-induced long-term potentiation (LTP) ex vivo. In the present study, we further examined the molecular mechanisms underlying the HFS-induced presynaptic LTP. We found that a presynaptic elevation of Ca²⁺ was required for the LTP induction. Interestingly, the blockade of presynaptic but not postsynaptic HCN channels with ZD7288 completely abolished LTP induction. While ZD7288 did not alter basal synaptic transmission, the blocker fully reversed previously established LTP, indicating that HCN channels are also required for the maintenance of LTP. Indeed, HCN3 and HCN4 channels were preferentially localized in the presynaptic boutons of LA afferents. Furthermore, an inhibition of either GABAB receptors or GIRK channels eliminated the inhibitory effect of HCN blockade on the LTP induction. Collectively, we suggest that activation of presynaptic HCN channels may counteract membrane hyperpolarization during tetanic stimulation, and thereby contributes to the presynaptic LTP at LA-BA synapses.
Auditory fear conditioning facilitates neurotransmitter release at lateral amygdala to basal amygdala synapses
2021, Biochemical and Biophysical Research Communications
Citation Excerpt :
Expression of conditioned fear depends on the CEm, a main output nucleus of the amygdala, eventually projecting to downstream fear effector structure, e.g., the periaqueductal gray [3]. The BA is positioned to relay CS-related information from the LA to the CeM [3,5–7]. Interestingly, BA lesions after conditioning completely abolished conditioned fear responses, but the lesioned rats were able to acquire a new conditioned fear [18].
The lateral amygdala (LA) is a main sensory input site from the cortical and thalamic regions. In turn, LA glutamatergic pyramidal neurons strongly project to the basal amygdala (BA). Although it is well known that auditory fear conditioning involves synaptic potentiation in the LA, it is not clear whether the LA-BA synaptic transmission is modified upon auditory fear conditioning. Here we found that high-frequency stimulation ex vivo resulted in long-term potentiation (LTP) with a concomitant enhancement of neurotransmitter release at LA-BA synapses. Auditory fear conditioning also led to the presynaptic facilitation at LA-BA synapses. Meanwhile, AMPA/NMDA current ratio was not changed upon fear conditioning, excluding the involvement of postsynaptic mechanism. Notably, fear conditioning occluded electrically induced ex vivo LTP in the LA-BA pathway, indicating that the conditioning and electrically induced LTP share common mechanisms. Our findings suggest that the presynaptic potentiation of LA-BA synapses may be involved in fear conditioning.
Different Multidimensional Representations across the Amygdalo-Prefrontal Network during an Approach-Avoidance Task
2020, Neuron
The prelimbic (PL) area and basolateral amygdala (lateral [LA] and basolateral [BL] nuclei) have closely related functions and similar extrinsic connectivity. Reasoning that the computational advantage of such redundancy should be reflected in differences in how these structures represent information, we compared the coding properties of PL and amygdala neurons during a task that requires rats to produce different conditioned defensive or appetitive behaviors. Rather than unambiguous regional differences in the identities of the variables encoded, we found gradients in how the same variables are represented. Whereas PL and BL neurons represented many different parameters through minor variations in firing rates, LA cells coded fewer task features with stronger changes in activity. At the population level, whereas valence could be easily distinguished from amygdala activity, PL neurons could distinguish both valence and trial identity as well as or better than amygdala neurons. Thus, PL has greater representational capacity.
Functional neuroanatomy of the basolateral amygdala: Neurons, neurotransmitters, and circuits
2020, Handbook of Behavioral Neuroscience
Citation Excerpt :
Both subdivisions of BM have strong projections to CM and CLC (Petrovich et al., 1996; Savander, Go, Ledoux, & Pitkänen, 1996). EM studies in cat indicate that BNC projections to the CeA mainly target spines and distal dendrites of spiny projection neurons (Paré, Smith, et al., 1995; Smith & Paré, 1994). The monkey LA has no significant projection to either of the two main subdivisions of the central nucleus (CM, medial subdivision; CL, lateral subdivision) (Fudge & Tucker, 2009).
The basolateral nuclear complex (BNC) of the amygdala consists of lateral, basolateral, and basomedial nuclei in the rat, and homologous nuclei in the monkey (lateral, basal, and accessory basal). There are two main types of neurons in the BNC: pyramidal neurons and nonpyramidal neurons. Although these cells do not exhibit a laminar organization, their morphology, synaptology, electrophysiology, and pharmacology are remarkably similar to their counterparts in the cerebral cortex. Like the cortex, there are several distinct interneuronal subpopulations in the BNC. Collectively, the nuclei of the BNC receive information from all sensory modalities, and via projections to the central amygdalar nucleus, bed nucleus of the stria terminalis, striatum, hypothalamus, and prefrontal cortex elicit emotional behavior. The BNC also plays a critical role in the formation and extinction of emotional memories. This review summarizes the organization of the local and extrinsic connections of BNC neurons that underly these functions.
Diverse glutamatergic inputs target spines expressing M1 muscarinic receptors in the basolateral amygdala: An ultrastructural analysis
2019, Brain Research
Although it is known that acetylcholine acting through M1 muscarinic receptors (M1Rs) is essential for memory consolidation in the anterior basolateral nucleus of the amygdala (BLa), virtually nothing is known about the circuits involved. In the hippocampus M1R activation facilitates long-term potentiation (LTP) by potentiating NMDA glutamate receptor (NMDAR) currents. The majority of NMDAR+ profiles in the BLa are spines. Since about half of dendritic spines of BLa pyramidal neurons (PNs) receiving glutamatergic inputs are M1R-immunoreactive (M1R+) it is possible that the role of M1Rs in BLa mnemonic functions also involves potentiation of NMDAR currents in spines. However, the finding that only about half of BLa spines are M1R+ suggests that this proposed mechanism may only apply to a subset of glutamatergic inputs. As a first step in the identification of differential glutamatergic inputs to M1R+ spines in the BLa, the present electron microscopic study used antibodies to two different vesicular glutamate transporter proteins (VGluTs) to label two different subsets of glutamatergic inputs to M1R+ spines. These inputs are largely complimentary with VGluT1+ inputs arising mainly from cortical structures and the basolateral nucleus, and VGluT2+ inputs arising mainly from the thalamus. It was found that about one-half of the spines that were postsynaptic to VGluT1+ or VGluT2+ terminals were M1R+. In addition, a subset of the VGluT1+ or VGluT2+ axon terminals were M1R+, including those that synapsed with M1R+ spines. These results suggest that acetylcholine can modulate glutamatergic inputs to BLa spines by presynaptic as well as postsynaptic M1R-mediated mechanisms.
A Tradeoff in the Neural Code across Regions and Species
2019, Cell
Many evolutionary years separate humans and macaques, and although the amygdala and cingulate cortex evolved to enable emotion and cognition in both, an evident functional gap exists. Although they were traditionally attributed to differential neuroanatomy, functional differences might also arise from coding mechanisms. Here we find that human neurons better utilize information capacity (efficient coding) than macaque neurons in both regions, and that cingulate neurons are more efficient than amygdala neurons in both species. In contrast, we find more overlap in the neural vocabulary and more synchronized activity (robustness coding) in monkeys in both regions and in the amygdala of both species. Our findings demonstrate a tradeoff between robustness and efficiency across species and regions. We suggest that this tradeoff can contribute to differential cognitive functions between species and underlie the complementary roles of the amygdala and the cingulate cortex. In turn, it can contribute to fragility underlying human psychopathologies.

View all citing articles on Scopus

View full text

Intra-amygdaloid projections of the basolateral and basomedial nuclei in the cat: Phaseolus vulgaris-leucoagglutinin anterograde tracing at the light and electron microscopic level

Abstract

Brain Res.

Prog. Neurobiol.

Brain Res.

Brain Res. Bull.

Brain Res.

Brain Res.

Physiol. Behav.

Neuroscience

Brain Res. Bull.

Neuroscience

Neuroscience

Neurosci. Lett.

Brain Res.

Neurosci. Lett.

A description of intra-amygdaloid connections in old world monkeys

Expl Brain Res.

Anatomical organization of the primate amygdaloid complex

Spatial relationships between the terminations of somatic sensory and motor pathways in the rostral brainstem of cats and monkeys. I. Ascending somatic sensory inputs to lateral diencephalon

J. comp. Neurol.

Immunocytochemical localization of glutamate decarboxylase in the rat basolateral amygdaloid nucleus, with special reference to GABAergic innervation of amygdalostriatal projection neurons

J. comp. Neurol.

Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex

J. Neurosci.

The electron-microscopic analysis of the neuronal organization of the cerebral cortex

The role of amygdaloid central nucleus in differential Pavlovian conditioning of bradycardia in rabbits

Behav. Brain Res.

The amygdala of the cat: a Golgi study

Z. Zellforsch.

Sensitization of the startle reflex by footshock: blockade by lesions of the central nucleus of the amygdala or its efferent pathway to the brainstem

Behav. Neurosci.

Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat

Expl Brain Res.