Long-term potentiation (LTP) which has long been considered a cellular model for learning and memory is defined as a lasting enhancement in synaptic transmission efficacy. This cellular mechanism has been demonstrated reliably in the hippocampus and the amygdala—two limbic structures implicated in learning and memory. Earlier studies reported on the ability of cortical stimulation of the entorhinal cortex to induce LTP simultaneously in the two sites. However, to retain a stable baseline of comparison with the majority of the LTP literature, it is important to investigate the ability of fiber stimulation such as perforant path activation to induce LTP concurrently in both structures. Therefore, in this paper we report on concurrent LTP in the basolateral amygdala (BLA) and the dentate gyrus (DG) subfield of the hippocampus induced by theta burst stimulation of perforant path fibers in freely behaving Sprague-Dawley rats. Our results indicate that while perforant path-evoked potentials in both sites exhibit similar triphasic waveforms, the latency and amplitude of BLA responses were significantly shorter and smaller than those of DG. In addition, we observed no significant differences in either the peak level or the duration of LTP between DG and BLA. 1. Introduction Long-term potentiation (LTP), a form of synaptic plasticity, is an activity-dependent increase in synaptic strength induced by high frequency stimulation of afferent pathways [1]. Owing to its associativity, specificity, and persistence properties LTP is now widely considered as a cellular model for learning and memory [2–5]. Much attention in LTP research has focused on the hippocampus which is thought to be involved in learning and memory processes. More recently, the amygdala has enjoyed renewed interest due to its implication in modulating synaptic plasticity in the hippocampus, the prefrontal cortex, and the anterior cingulate cortex [6–9] and its involvement in memory consolidation and emotional memories [10–17]. Emotional memories, including fear conditioning and extinction, are thought to be mediated by the amygdala [10, 18–21]. The basolateral amygdala (BLA) in particular has been shown to be extensively connected with cortical and subcortical structures involved in memory and emotion, notably the hippocampal formation, the striatum, the prefrontal cortex, the entorhinal cortex, the association cortices, and the thalamus, among others [22, 23]. As a result, the BLA is thought to play a crucial role in psychophysiological responses to emotionally salient events or sensory stimuli
References
[1]
T. V. P. Bliss and T. Lomo, “Long lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path,” Journal of Physiology, vol. 232, no. 2, pp. 331–356, 1973.
[2]
S. J. Martin, P. D. Grimwood, and R. G. M. Morris, “Synaptic plasticity and memory: an evaluation of the hypothesis,” Annual Review of Neuroscience, vol. 23, pp. 649–711, 2000.
[3]
T. V. P. Bliss and G. L. Collingridge, “A synaptic model of memory: Long-term potentiation in the hippocampus,” Nature, vol. 361, no. 6407, pp. 31–39, 1993.
[4]
R. C. Malenka and R. A. Nicoll, “Long-term potentiation—a decade of progress?” Science, vol. 285, no. 5435, pp. 1870–1874, 1999.
[5]
W. C. Abraham and J. M. Williams, “Properties and mechanisms of LTP maintenance,” Neuroscientist, vol. 9, no. 6, pp. 463–474, 2003.
[6]
Y. Ikegaya, H. Saito, and K. Abe, “High-frequency stimulation of the basolateral amygdala facilitates the induction of long-term potentiation in the dentate gyrus in vivo,” Neuroscience Research, vol. 22, no. 2, pp. 203–207, 1995.
[7]
I. Akirav and G. Richter-Levin, “Mechanisms of amygdala modulation of hippocampal plasticity,” Journal of Neuroscience, vol. 22, no. 22, pp. 9912–9921, 2002.
[8]
G. Bush, P. Luu, and M. I. Posner, “Cognitive and emotional influences in anterior cingulate cortex,” Trends in Cognitive Sciences, vol. 4, no. 6, pp. 215–222, 2000.
[9]
M. Davis, J. M. Hitchcock, M. B. Bowers, C. W. Berridge, K. R. Melia, and R. H. Roth, “Stress-induced activation of prefrontal cortex dopamine turnover: blockade by lesions of the amygdala,” Brain Research, vol. 664, no. 1-2, pp. 207–210, 1994.
[10]
J. E. LeDoux, “Emotion circuits in the brain,” Annual Review of Neuroscience, vol. 23, pp. 155–184, 2000.
[11]
J. L. McGaugh, “Memory consolidation and the amygdala: a systems perspective,” Trends in Neurosciences, vol. 25, no. 9, pp. 456–461, 2002.
[12]
J. L. McGaugh, “The amygdala modulates the consolidation of memories of emotionally arousing experiences,” Annual Review of Neuroscience, vol. 27, pp. 1–28, 2004.
[13]
D. Paré, “Role of the basolateral amygdala in memory consolidation,” Progress in Neurobiology, vol. 70, no. 5, pp. 409–420, 2003.
[14]
B. Roozendaal, “Systems mediating acute glucocorticoid effects on memory consolidation and retrieval,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 27, no. 8, pp. 1213–1223, 2003.
[15]
L. Cahill and J. L. McGaugh, “Modulation of memory storage,” Current Opinion in Neurobiology, vol. 6, no. 2, pp. 237–242, 1996.
[16]
C. K. McIntyre, T. Miyashita, B. Setlow et al., “Memory-influencing intra-basolateral amygdala drug infusions modulate expression of Arc protein in the hippocampus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 30, pp. 10718–10723, 2005.
[17]
H. Eichenbaum, T. Otto, and N. J. Cohen, “The hippocampus—what does it do?” Behavioral and Neural Biology, vol. 57, no. 1, pp. 2–36, 1992.
[18]
S. Maren, “Nuerobiology of Pavlovian fear conditioning,” Annual Review of Neuroscience, vol. 24, pp. 897–931, 2001.
[19]
J. L. McGaugh, C. K. McIntyre, and A. E. Power, “Amygdala modulation of memory consolidation: interaction with other brain systems,” Neurobiology of Learning and Memory, vol. 78, no. 3, pp. 539–552, 2002.
[20]
K. S. LaBar and R. Cabeza, “Cognitive neuroscience of emotional memory,” Nature Reviews Neuroscience, vol. 7, no. 1, pp. 54–64, 2006.
[21]
E. A. Phelps, M. R. Delgado, K. I. Nearing, and J. E. Ledoux, “Extinction learning in humans: role of the amygdala and vmPFC,” Neuron, vol. 43, no. 6, pp. 897–905, 2004.
[22]
A. J. Mcdonald, “Cortical pathways to the mammalian amygdala,” Progress in Neurobiology, vol. 55, no. 3, pp. 257–332, 1998.
[23]
C. B. Canto, F. G. Wouterlood, and M. P. Witter, “What does the anatomical organization of the entorhinal cortex tell us?” Neural Plasticity, vol. 2008, Article ID 381243, 18 pages, 2008.
[24]
M. G. Packard and L. Cahill, “Affective modulation of multiple memory systems,” Current Opinion in Neurobiology, vol. 11, no. 6, pp. 752–756, 2001.
[25]
L. Cahill and J. L. McGaugh, “Mechanisms of emotional arousal and lasting declarative memory,” Trends in Neurosciences, vol. 21, no. 7, pp. 294–299, 1998.
[26]
A. Kavushansky, R. M. Vouimba, H. Cohen, and G. Richter-Levin, “Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress,” Hippocampus, vol. 16, no. 1, pp. 35–42, 2006.
[27]
R. M. Vouimba, D. Yaniv, D. Diamond, and G. Richter-Levin, “Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats,” European Journal of Neuroscience, vol. 19, no. 7, pp. 1887–1894, 2004.
[28]
D. Yaniv, R. M. Vouimba, D. M. Diamond, and G. Richter-Levin, “Simultaneous induction of long-term potentiation in the hippocampus and the amygdala by entorhinal cortex activation: mechanistic and temporal profiles,” Neuroscience, vol. 120, no. 4, pp. 1125–1135, 2003.
[29]
K. J. Canning and L. S. Leung, “Lateral entorhinal, perirhinal, and amygdala-entorhinal transition projections to hippocampal CA1 and dentate gyrus in the rat: a current source density study,” Hippocampus, vol. 7, no. 6, pp. 643–655, 1997.
[30]
D. P. Cain, F. Boon, and E. L. Hargreaves, “Evidence for different neurochemical contributions to long-term potentiation and to kindling and kindling-induced potentiation: role of NMDA and urethane-sensitive mechanisms,” Experimental Neurology, vol. 116, no. 3, pp. 330–338, 1992.
[31]
M. B. MacIver, D. L. Tauck, and J. J. Kendig, “General anaesthetic modification of synaptic facilitation and long-term potentiation in hippocampus,” British Journal of Anaesthesia, vol. 62, no. 3, pp. 301–310, 1989.
[32]
M. E. Gilbert and C. M. Mack, “Field potential recordings in dentate gyrus of anesthetized rats: stability of baseline,” Hippocampus, vol. 9, no. 3, pp. 277–287, 1999.
[33]
T. J. Shors and E. Dryver, “Effect of stress and long-term potentiation (LTP) on subsequent LTP and the theta burst response in the dentate gyrus,” Brain Research, vol. 666, no. 2, pp. 232–238, 1994.
[34]
W. C. Abraham, S. E. Mason-Parker, M. F. Bear, S. Webb, and W. P. Tate, “Heterosynaptic metaplasticity in the hippocampus in vivo: a BCM-like modifiable threshold for LTP,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 19, pp. 10924–10929, 2001.
[35]
S. Maren, “Sexually dimorphic perforant path long-term potentiation (LTP) in urethane-anesthetized rats,” Neuroscience Letters, vol. 196, no. 3, pp. 177–180, 1995.
[36]
R. Freudenthal, A. Romano, and A. Routtenberg, “Transcription factor NF-κB activation after in vivo perforant path LTP in mouse hippocampus,” Hippocampus, vol. 14, no. 6, pp. 677–683, 2004.
[37]
J. H. Blaise, J. L. Koranda, U. Chow, K. E. Haines, and E. C. Dorward, “Neonatal isolation stress alters bidirectional long-term synaptic plasticity in amygdalo-hippocampal synapses in freely behaving adult rats,” Brain Research, vol. 1193, no. C, pp. 25–33, 2008.
[38]
E. L. Hargreaves, D. P. Cain, and C. H. Vanderwolf, “Learning and behavioral-long-term potentiation: importance of controlling for motor activity,” Journal of Neuroscience, vol. 10, no. 5, pp. 1472–1478, 1990.
[39]
J. Winson and C. Abzug, “Neuronal transmission through hippocampal pathways dependent on behavior,” Journal of Neurophysiology, vol. 41, no. 3, pp. 716–732, 1978.
[40]
V. Aroniadou-Anderjaska, R. M. Post, M. A. Rogawski, and H. Li, “Input-specific LTP and depotentiation in the basolateral amygdala,” NeuroReport, vol. 12, no. 3, pp. 635–640, 2001.
[41]
S. C. Stanford, “Central noradrenergic neurones and stress,” Pharmacology and Therapeutics, vol. 68, no. 2, pp. 297–342, 1995.
[42]
R. Galvez, M. H. Mesches, and J. L. Mcgaugh, “Norepinephrine release in the amygdala in response to footshock stimulation,” Neurobiology of Learning and Memory, vol. 66, no. 3, pp. 253–257, 1996.
[43]
G. L. Quirarte, R. Galvez, B. Roozendaal, and J. L. McGaugh, “Norepinephrine release in the amygdala in response to footshock and opioid peptidergic drugs,” Brain Research, vol. 808, no. 2, pp. 134–140, 1998.
[44]
M. Tanaka, M. Yoshida, H. Emoto, and H. Ishii, “Noradrenaline systems in the hypothalamus, amygdala and locus coeruleus are involved in the provocation of anxiety: basic studies,” European Journal of Pharmacology, vol. 405, no. 1–3, pp. 397–406, 2000.
[45]
V. Aroniadou-Anderjaska, F. Qashu, and M. F. M. Braga, “Mechanisms regulating GABAergic inhibitory transmission in the basolateral amygdala: implications for epilepsy and anxiety disorders,” Amino Acids, vol. 32, no. 3, pp. 305–315, 2007.
[46]
D. J. Berlau and J. L. McGaugh, “Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basolateral amygdala,” Neurobiology of Learning and Memory, vol. 86, no. 2, pp. 123–132, 2006.
[47]
A. J. McDonald and F. Mascagni, “Projections of the lateral entorhinal cortex to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat,” Neuroscience, vol. 77, no. 2, pp. 445–459, 1997.
[48]
S. Maren and M. S. Fanselow, “Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo,” Journal of Neuroscience, vol. 15, no. 11, pp. 7548–7564, 1995.
