Complex sensory properties of certain amygdala units in the freely moving cat

doi:10.1016/0014-4886(69)90086-7

Experimental Neurology

Volume 23, Issue 3, March 1969, Pages 384-398

https://doi.org/10.1016/0014-4886(69)90086-7 Get rights and content

Abstract

In the freely moving cat, sensory properties of amygdala units were studied for extended periods. Seven out of sixty units responded selectively to complex sensory stimuli such as simulated bird calls or a black mouse. The responses of these units did not change during behavioral habituation and only rarely were they influenced by changes in the alertness or emotional state of the animal. It is concluded that there are cells in the amygdala that abstract from the sensory array information which represents “things” in the external world. A few units showed after-responses following termination of the stimulus. These may be involved in maintaining behavior after sensory stimulation.

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In the awake rat, two distinct types of basolateral amygdala neurons were found to encode either palatability or rewarding properties of tasting (Fontanini, Grossman, Figueroa, & Katz, 2009). Amygdala neurons are often activated by presumably neutral visual stimuli in awake cats and rats, such as light flashes, striped card, rubber hose (Machne & Segundo, 1956; O'Keefe & Bouma, 1969; Pascoe & Kapp, 1985b; Uwano et al., 1995), and in monkeys, by stimuli such as tape, glove, bottle, or fork (Nishijo, Ono, & Nishino, 1988a; Wilson & Rolls, 1993). Neurons are also activated, often to a greater degree, by biologically relevant visual stimuli in awake cats and monkeys, such as a live mouse, live rat, food, and an air puff bulb (Jacobs & McGinty, 1971, 1972; O'Keefe & Bouma, 1969; Sanghera, Rolls, & Roper-Hall, 1979; Sawa & Delgado, 1963; Wilson & Rolls, 1993).
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Further, the amygdala is involved in disorders that include an altered emotional response to speech, such as schizophrenia (Sanjuan et al., 2007; Escarti et al., 2010), autism (Gabis et al., 2008; Kim et al., 2010), and some forms of post-traumatic stress (Protopopescu et al., 2005; Shin et al., 2006). In other species, early work showed that amygdalar neurons respond to social vocalizations (Sawa and Delgado, 1963; O’Keefe and Bouma, 1969; Jacobs and McGinty, 1972), but there have been few systematic studies of responses to social vocalizations by amygdalar neurons. In recent work on mustached bats (Naumann and Kanwal, 2011), big brown bats (Gadziola et al., 2012), and rats (Parsana et al., 2012), conspecific vocal signals evoked a variety of temporal response patterns among basolateral amygdalar neurons, but neurons generally showed stronger excitatory discharge in response to vocal signals with negative affect.
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The LHA represents US value, sending excitatory projections onto dopamine cells, while the VS neurons come to inhibit a dopamine burst that the LHA would otherwise cause once that US becomes “expected.” The excitatory component of the LV system (LVe) is associated with the central nucleus of the amygdala (CNA; Fuster and Uyeda, 1971; Miller, 2000; O’Keefe and Bouma, 1969; Ono et al., 1995; Sanghera et al., 1979; Schultz and Romo, 1990), which can learn stimulus associations to reward outcomes, and drive dopamine firing through excitatory projections of its own to the VTA and SNc. In a simple Pavlovian conditioning paradigm, these brain areas interact as follows.
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¹: This work was supported by Contract SD-193 of the U. S. Department of Defense to Dr. Ronald Melzack. Dr. O'Keefe, now in the M.R.C. Cerebral Functions Research Group, Department of Anatomy, University College London, Gower St., London, W.C.1., England, was supported by a U.S.N.I.M.H. predoctoral grant and Dr. Bouma, who was on leave from the Institute for Perception Research, Eindhoven, the Netherlands, was supported by a grant from the Netherlands Organization for the Advancement of Pure Research (Z.W.O.). The authors thank Mr. Daniel Frank for his help in the early phases of this research and Dr. Melzack for his support and encouragement.

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Complex sensory properties of certain amygdala units in the freely moving cat

Abstract

Electroencephalog. Clin. Neurophysiol.

Contrasting effects of two identified amygdaloid efferent pathways on single hypothalamic neurons

J. Neurophysiol.

Response patterns elicited from the amygdala and deep temporoinsular cortex

Amygdala

Functions of the amygdala

Psych. Bull.

Rapid procedure to localize electrodes in experimental neurophysiology

Biol. Inst. Estud. Med. Biol. Mex.

Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat

J. Neurophysiol.

Unitary responses to afferent volleys in amygdaloid complex

J. Neurophysiol.