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PLOS ONE  2011 

Patterns of Coupled Theta Activity in Amygdala-Hippocampal-Prefrontal Cortical Circuits during Fear Extinction

DOI: 10.1371/journal.pone.0021714

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Abstract:

Signals related to fear memory and extinction are processed within brain pathways involving the lateral amygdala (LA) for formation of aversive stimulus associations, the CA1 area of the hippocampus for context-dependent modulation of these associations, and the infralimbic region of the medial prefrontal cortex (mPFC) for extinction processes. While many studies have addressed the contribution of each of these modules individually, little is known about their interactions and how they function as an integrated system. Here we show, by combining multiple site local field potential (LFP) and unit recordings in freely behaving mice in a fear conditioning paradigm, that theta oscillations may provide a means for temporally and functionally connecting these modules. Theta oscillations occurred with high specificity in the CA1-LA-mPFC network. Theta coupling increased between all areas during retrieval of conditioned fear, and declined during extinction learning. During extinction recall, theta coupling partly rebounded in LA-mPFC and CA1-mPFC, and remained at a low level in CA1-LA. Interfering with theta coupling through local electrical microstimulation in CA1-LA affected conditioned fear and extinction recall depending on theta phase. These results support the hypothesis that theta coupling provides a means for inter-areal coordination in conditioned behavioral responsiveness. More specifically, theta oscillations seem to contribute to a population code indicating conditioned stimuli during recall of fear memory before and after extinction.

References

[1]  LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23: 155–84. 155-184.
[2]  Maren S, Quirk GJ (2004) Neuronal signalling of fear memory. Nat Rev Neurosci 5: 844–852.
[3]  Myers KM, Davis M (2007) Mechanisms of fear extinction. Mol Psychiatry 12: 120–150.
[4]  Sehlmeyer C, Schoning S, Zwitserlood P, Pfleiderer B, Kircher T, et al. (2009) Human fear conditioning and extinction in neuroimaging: a systematic review. PLoS One 4: e5865.
[5]  Ji J, Maren S (2007) Hippocampal involvement in contextual modulation of fear extinction. Hippocampus 17: 749–758.
[6]  Quirk GJ, Mueller D (2008) Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33: 56–72.
[7]  Buzsaki G (2005) Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15: 827–840.
[8]  Magee JC, Johnston D (1995) Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268: 301–304.
[9]  Jensen O, Lisman JE (1996) Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn Mem 3: 279–287.
[10]  Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6: 149–172.
[11]  Dragoi G, Buzsaki G (2006) Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50: 145–157.
[12]  Buzsaki G (2002) Theta oscillations in the hippocampus. Neuron 33: 325–340.
[13]  Pare D, Gaudreau H (1996) Projection cells and interneurons of the lateral and basolateral amygdala: distinct firing patterns and differential relation to theta and delta rhythms in conscious cats. J Neurosci 16: 3334–3350.
[14]  Pare D, Collins DR (2000) Neuronal correlates of fear in the lateral amygdala: multiple extracellular recordings in conscious cats. J Neurosci 20: 2701–2710.
[15]  Siapas AG, Lubenov EV, Wilson MA (2005) Prefrontal phase locking to hippocampal theta oscillations. Neuron 46: 141–151.
[16]  Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, et al. (2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60: 683–697.
[17]  Paz R, Bauer EP, Pare D (2008) Theta synchronizes the activity of medial prefrontal neurons during learning. Learn Mem 15: 524–531.
[18]  Sangha S, Narayanan RT, Bergado-Acosta JR, Stork O, Seidenbecher T, et al. (2009) Deficiency of the 65 kDa isoform of glutamic acid decarboxylase impairs extinction of cued but not contextual fear memory. J Neurosci 29: 15713–15720.
[19]  Adhikari A, Topiwala MA, Gordon JA (2010) Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 65: 257–269.
[20]  Seidenbecher T, Laxmi TR, Stork O, Pape HC (2003) Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301: 846–850.
[21]  Narayanan RT, Seidenbecher T, Sangha S, Stork O, Pape HC (2007) Theta resynchronization during reconsolidation of remote contextual fear memory. Neuroreport 18: 1107–1111.
[22]  Narayanan RT, Seidenbecher T, Kluge C, Bergado J, Stork O, et al. (2007) Dissociated theta phase synchronization in amygdalo- hippocampal circuits during various stages of fear memory. Eur J Neurosci 25: 1823–1831.
[23]  Popa D, Duvarci S, Popescu AT, Lena C, Pare D (2010) Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep. Proc Natl Acad Sci U S A 107: 6516–6519.
[24]  Pape HC, Narayanan RT, Smid J, Stork O, Seidenbecher T (2005) Theta activity in neurons and networks of the amygdala related to long-term fear memory. Hippocampus 15: 874–880.
[25]  Lesting J, Geiger M, Narayanan RT, Pape HC, Seidenbecher T (2011) Impaired extinction of fear and maintained amygdala-hippocampal theta synchrony in a mouse model of temporal lobe epilepsy. Epilepsia 52: 337–346.
[26]  Fink AE, O'Dell TJ (2009) Short trains of theta frequency stimulation enhance CA1 pyramidal neuron excitability in the absence of synaptic potentiation. J Neurosci 29: 11203–11214.
[27]  Farinelli M, Deschaux O, Hugues S, Thevenet A, Garcia R (2006) Hippocampal train stimulation modulates recall of fear extinction independently of prefrontal cortex synaptic plasticity and lesions. Learn Mem 13: 329–334.
[28]  Mizuseki K, Sirota A, Pastalkova E, Buzsaki G (2009) Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 64: 267–280.
[29]  Rodrigues SM, Schafe GE, LeDoux JE (2004) Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44: 75–91.
[30]  Pape HC, Pare D (2010) Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 90: 419–463.
[31]  Malenka RC (2003) The long-term potential of LTP. Nat Rev Neurosci 4: 923–926.
[32]  Quirk GJ, Repa C, LeDoux JE (1995) Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron 15: 1029–1039.
[33]  Hugues S, Garcia R (2007) Reorganization of learning-associated prefrontal synaptic plasticity between the recall of recent and remote fear extinction memory. Learn Mem 14: 520–524.
[34]  Repa JC, Muller J, Apergis J, Desrochers TM, Zhou Y, et al. (2001) Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat Neurosci 4: 724–731.
[35]  Herry C, Ciocchi S, Senn V, Demmou L, Muller C, et al. (2008) Switching on and off fear by distinct neuronal circuits. Nature 454: 600–606.
[36]  Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106: 274–285.
[37]  Corcoran KA, Maren S (2001) Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. J Neurosci 21: 1720–1726.
[38]  Maren S, Hobin JA (2007) Hippocampal regulation of context-dependent neuronal activity in the lateral amygdala. Learn Mem 14: 318–324.
[39]  Franklin KBJ, Paxinos G (1997) The Mouse Brain in Stereotaxic Coordinates. San Diego: Academic Press.

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