Elsevier

Physiology & Behavior

Volume 77, Issues 4–5, December 2002, Pages 489-493
Physiology & Behavior

Regulation of conditioned responses of basolateral amygdala neurons

https://doi.org/10.1016/S0031-9384(02)00909-5Get rights and content

Abstract

The basolateral amygdala (BLA) is a component of a system that drives and modulates affective behavior. Some forms of affective behavior are regulated by the prefrontal cortex (PFC) and enhanced by dopamine (DA). By using intracellular and extracellular electrophysiological techniques in anesthetized rats, our studies attempt to uncover cellular mechanisms that allow for regulation of affect by PFC-induced inhibition of BLA output and plasticity, as well as mechanisms by which DA enhances affective behavior via modulation of BLA neuronal excitability, afferent input and plasticity. We have found that stimulation of medial PFC (mPFC) results in a profound inhibition of BLA output, manifest as a suppression of spontaneous, intracellular current-driven or sensory cortical afferent-driven spike firing of BLA projection neurons. This inhibition is mediated by excitation of GABAergic interneurons of the BLA. Activation of DA receptors attenuates this inhibitory action of the mPFC, while enhancing other (i.e., sensory-related) inputs by increases in postsynaptic excitability of BLA projection neurons. Furthermore, Pavlovian conditioning procedures that pair an odor with a footshock result in enhanced odor-evoked postsynaptic potentials. This plasticity of odor-evoked responses is blocked by antagonism of DA receptors and by stimulation of mPFC. Our data indicate that the mPFC exerts regulatory control over BLA via suppression of spontaneous and sensory-driven activity, as well as BLA plasticity. Activation of DA receptors suppresses the inhibitory influence of the mPFC, allowing sensory-driven BLA activity and plasticity. Functionally, in the presence of high DA levels, which suppresses mPFC-evoked inhibition, one source of affective control will be dampened. Furthermore, sensory-related inputs will be further enhanced by the increased excitability of BLA neurons. This situation is expected to maximize affective responses to sensory stimuli, as well as plasticity.

Section snippets

Afferent regulation of the amygdala

The amygdala is divided into a number of subregions. Two of these subregions are of particular interest to our laboratory: (1) the basolateral amygdala (BLA)—this region is comprised of principal output neurons that are glutamatergic, pyramidal-shaped neurons, and provide excitatory output to a number of rostral brain regions, including the accumbens and the prefrontal cortex (PFC); (2) the central nucleus (CeA)—this region contains primarily GABAergic neurons that project to brainstem

Prefrontal regulation of BLA responses: a functional consideration

Conceptually, we propose that the interaction of PFC afferents in the BLA may provide insight regarding how information is processed within the BLA. Thus, the presentation of a complex sensory stimulus (such as the sound of a dog barking) would be expected to evoke an emotional response by activation of the excitatory association cortical afferents to the BLA that, in turn, would suppress activity within the CeA and thereby disinhibit subcortical areas. This would include CeA projection sites

Dopamine (DA) modulation of BLA responses

The response of BLA neurons to sensory cortical stimulation was also found to be potently affected by alterations of the mesolimbic DA system. Thus, our studies show that pharmacological manipulation of DA receptors exerts multiple actions within the BLA of anesthetized rats. DA acting via D2 receptors was found to cause a potentiation of sensory cortical afferents, apparently mediated via an increase in the input resistance of the membrane (Fig. 1). As a consequence, D2 stimulation would be

Modulation of conditioned responses within the BLA

In addition to short-term modulation, the amygdala also exhibits conditioning [27], [28]. Our studies have shown that such conditioned responses can be evaluated using intracellular recording in vivo from the anesthetized rat. As reviewed above, the BLA shows activation by various stimuli. Thus, presentation of an odor to the rat's nose will evoke EPSPs in the membrane of BLA neurons. If this odor is presented repeatedly, the amplitude of the EPSPs will decrease to the point where the odor

Regulation of BLA plasticity and its relationship to schizophrenia pathophysiology

These results show that the BLA is capable of exhibiting conditioned responses on a single-neuron level, even when the animal is anesthetized. This conditioning will alter the manner in which the BLA neuron responds to normally benign stimuli, if the stimulus is paired with a potent stressor under the appropriate conditions. These conditions include stimulation by DA, as well as a lack of suppressive influence by the PFC (Fig. 3). Thus, the PFC is capable of preventing such conditioning, most

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