The characteristics of the operation of the amygdalar neural network in unconditioned fear were identified by studying the interactions and nature of the spike activity of individual neurons in the basal and central nuclei of the amygdala in rabbits during freezing (fear), active unconditioned motor reactions (absence of fear), and in response to emotionally significant stimuli, as well as in calm waking. When rabbits froze, there were specific changes in the interactions of close-lying amygdalar neurons as compared with other states; these changes were not seen in the spike activity of individual neurons. Freezing increased the numbers of short-latency (up to 100 msec) excitatory connections and decreased the numbers of long-latency (250–450 msec) inhibitory connections. Neuron interactions were seen at frequencies in the delta2 range (2–4 Hz) more often in this state than in others. When the animals made active motor responses to the stimulus, there were decreases in the numbers of interacting neurons and increases in the numbers of longlatency (200–250 msec) excitatory and short-latency (50–200 msec) inhibitory connections, and a greater proportion of interactions occurred at frequencies of the theta1 range more frequently than in other states. Thus, the balance between the excitatory and inhibitory components of the amygdalar neural network is important for the occurrence of fear.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
P. Bogach and B. L. Ganzha, “High-frequency synchronized activity in the amygdala as an EEG parameter of a number of psychophysiological states,” in: Problems in Hypothalamic Physiology [in Russian], Universitet, Kiev (1973), pp. 3–18.
Y. Buresh, M. Petarn, and I. Zakhar, Electrophysiological Study Methods [Russian translation], Foreign Literature Press, Moscow (1962).
D. A. Zhukov, “The psychogenetics of stress,” in: Behavioral and Endocrine Correlates of Genetic Determinants of Stress Reactivity in Uncontrollable Situations [in Russian], St. Petersburg Center for Scientific and Technical Information, St. Petersburg (1996).
R. Yu. Ilyuchenok, M. A. Gilinskii, L. V. Loskutova, N. I. Dubrovina, and N. V. Volf, The Amygdaloid Complex (connections, behavior, memory) [in Russian], Nauka, Novosibirsk (1981).
I. V. Pavlova, “Interaction of neurons in the hippocampus and frontal cortex in emotionally negative situations in active and passive rabbits,” Zh. Vyssh. Nerv. Deyat., 59, No. 1, 75–86 (2009).
I. V. Pavlova, I. P. Levshina, G. L. Vanetsian,Yu. V. Pavlov, N. N. Shuikin, and E. A. Zyablitseva, “Effects of emotionally significant stimuli on behavior and respiration in rabbits with different movement activity in an open field,” Zh. Vyssh. Nerv. Deyat., 56, No. 1, 65–74 (2006).
P. V. Simonov, The Motivated Brain [in Russian], Nauka, Moscow (1987).
C. D. Applegate, R. C. Frysinger, B. S. Kapp, and M. Gallagher, “Multiple unit activity recorded from amygdale central nucleus during Pavlovian heart rate conditioning in rabbit,” Brain Res., 238, No. 2, 457–462 (1982).
D. J. Bailey, J. J. Kim, W. Sun, R. F. Thompson, and F. J. Helmstetter, “Acquisition of fear conditioning in rats requires synthesis of mRNA in the amygdala,” Behav. Neurosci., 113, No. 2, 276–282 (1999).
H. T. Blair, V. K. Huynh, V. T. Vaz, J. Van, R. R. Patel, A. K. Hiteshi, J. E. Lee, and J. W. Tapley, “Unilateral storage of fear memories by the amygdala,” J. Neurosci., 25, No. 16, 4198–4205 (2005).
D. R. Collins and D. Pare, “Differential fear conditioning induces reciprocal changes in the sensory responses of lateral amygdala neurons to the CS (+) and CS (–),” Learn. Mem., 7, No. 2, 97–103 (2000).
D. R. Collins, J. G. Pelletier, and D. Pare, “Slow and fast neuronal oscillation in the perirhinal cortex and lateral amygdale,” J. Neurophysiol., 85, No. 4, 1661–1672 (2001).
K. A. Goosens and S. Maren, “Contextual and auditory fear conditioning are mediated by the lateral, basal and central amygdaloid nuclei in rats,” Learn. Mem., 8, No. 3, 148–155 (2001).
J. M. Hitchcock and M. Davis, “Efferent pathway of the amygdala involved in conditioned fear as measured with the fear-potentiated startle paradigm,” Behav. Neurosci., 105, No. 6 826–842 (1991).
K. Jungling, T. Seidenbecher, L. Sosulina, J. Lesting, S. Sangha, S. D. Clark, N. Okamura, D. M. Duangdao, Y.-L. Xu, R. K. Reinscheid, and H. C. Pape, “Neuropeptide S-mediated control of fear expression and extinction: role of intercalated GABAergic neurons in the amygdala,” Neuron, 59, 298–310 (2008).
G. Liebsch, R. Landgraf, R. Gerstberger, J. C. Probst, C. T. Wotjak, M. Engelmann, F. Holsboer, and A. Montkowski, “Chronic infusion of a CHR1 receptor antisense oligodeoxynucleotide into the central nucleus of the amygdale reduced anxiety-related behavior in socially defeated rats,” Regul. Pept., 59, No. 2, 229–239 (1995).
C. E. Macedo, V. M. Castilho, M. A. De Souza e Silva, and M. L. Brandao, “Dual 5-HT mechanisms in basolateral and central nuclei of amygdale in the regulation of the defensive behavior induced by electrical stimulation of the inferior colliculus,” Brain Res. Bull., 59, No. 3, 189–195 (2002).
S. Maren, “Long-term potentiation in the amygdale: a mechanism for emotional learning and memory,” Trends Neurosci., 22, No. 12, 561–567 (1999).
S. Maren, “Auditory fear conditioning increases CS-elicited spike firing in lateral amygdale neurons even after extensive overtraining,” Eur. J. Neurosci., 12, No. 11, 4047–4054 (2000).
S. Maren, C. R. Ferrario, K. A. Corcoran, T. J. Desmond, and K. A. Frey, “Protein synthesis in the amygdala, but not the auditory thalamus, is required for consolidation of Pavlovian fear conditioning in rats,” Eur. J. Neurosci., 18, No. 11, 3080–3088 (2003).
A. Marowsky,Y. Yanagawa, K. Obata, and K. E. Vogt, “A specialized subclass of interneurons mediates dopaminergic facilitation of amygdala function,” Neuron, 48, No. 6, 1025–1037 (2005).
H. C. Pape, R. T. Narayanan, J. Smid, O. Stork, and T. Seidenbecher, “Theta activity in neurons and networks of the amygdale related to long-term fear memory,” Hippocampus, 15, No. 7, 874–880 (2005).
D. Pare and D. R. Collins, “Neuronal correlates of fear in the lateral amygdala: multiple extracellular recordings in conscious cats,” J. Neurosci., 20, No. 7, 2701–2710 (2000).
S. Royer and D. Pare, “Bidirectional synaptic plasticity in intercalated amygdale neurons and the extinction of conditioned fear responses,” Neurosci., 115, No. 2, 455–462 (2002).
C. Szinyei, R. T. Narayanan, and H. C. Pape, “Plasticity of inhibitory synaptic network interactions in the lateral amygdale upon fear conditioning in mice,” Eur. J. Neurosci., 25, No. 4, 1205–1211 (2007).
E. Tsvetkov, R. M. Shin, and V. Y. Bolshakov, “Glutamate uptake determines pathway specificity of long-term potentiation in the neural circuitry of fear conditioning,” Neuron, 41, No. 1, 139–151 (2004).
H. Van Lier, A. M. Coenen, and W. H. Drinkenburg, “Behavioral transitions modulate hippocampal electroencephalogram correlates of open field behavior in the rat: support for a sensorimotor function of hippocampal rhythmical synchronous activity,” J. Neurosci., 23, No. 6, 2459–2465 (2003).
A. Vazdarjanova, L. Cahill, and J. L. McGough, “Disrupting basolateral amygdale function impairs unconditioned freezing and avoidance in rats,” Eur. J. Neurosci., 14, No. 4, 709–718 (2001).
P. J. Whalen, S. L. Rauch, N. L. Etcoff, S. C. McInerney, M. B. Lee, and M. A. Henike, “Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge,” J. Neurosci., 18, No. 1, 411–418 (1998).
Y. H. Yu and W. W. Blessing, “Neurons in amygdala mediate ear pinna vasoconstriction elicited by unconditioned salient stimuli in conscious rabbits,” Auton. Neurosci., 87, No. 2–3, 236–242 (2001).
Author information
Authors and Affiliations
Corresponding author
Additional information
Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 59, No. 6, pp. 707–720, November–December, 2009.
Rights and permissions
About this article
Cite this article
Rysakova, M.P., Pavlova, I.V. Interactions and Firing Patterns of Rabbit Amygdalar Neurons in Unconditioned Fear Manifested as Freezing. Neurosci Behav Physi 41, 297–308 (2011). https://doi.org/10.1007/s11055-011-9416-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11055-011-9416-7