Abstract
Recognizing reward-related stimuli is crucial for survival. Neuronal projections from the basolateral amygdala (BLA) to the nucleus accumbens (NAc) play an important role in processing reward-related cues. Previous studies revealed synchronization between distant brain regions in reward-sensitive neurocircuits; however, whether the NAc synchronizes with the BLA is unknown. Here, we recorded local field potentials simultaneously from the BLA and NAc of rats during social preference tests and an appetitive conditioning test in which explicit stimuli were associated with food. BLA-NAc coherence in the theta band (5–8 Hz) increased in response to food-associated cues. Meanwhile, the modulatory strength of theta–high gamma (50–110 Hz) phase-amplitude cross-frequency coupling (PAC) in the NAc decreased. Importantly, both of these neuromodulations disappeared upon extinction. In contrast, both theta and gamma power oscillations in each region increased in the presence of social conspecifics or contexts associated with conspecifics, but coherence did not change. To potentially disrupt behavior and associated neural activity, a subgroup of rats was exposed prenatally to valproic acid (VPA), which has been shown to disrupt transcriptome and excitatory/inhibitory balance in the amygdala. VPA-exposed rats demonstrated impulsive-like behavior, but VPA did not affect BLA-NAc coherence. These findings reveal changes in BLA-NAc coherence in response to select reward-related stimuli (i.e., food-predictive cues); the differences between the tasks used here could shed light onto the functional nature of BLA-NAc coherence and are discussed.
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Adhikari A, Topiwala MA, Gordon JA (2010) Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 65:257–269
Amadei EA, Johnson ZV, Jun Kwon Y, Shpiner AC, Saravanan V, Mays WD, Ryan SJ, Walum H, Rainnie DG, Young LJ, Liu RC (2017) Dynamic corticostriatal activity biases social bonding in monogamous female prairie voles. Nature 546:297–301
Ambroggi F, Ishikawa A, Fields HL, Nicola SM (2008) Basolateral amygdala neurons facilitate reward-seeking behavior by exciting nucleus accumbens neurons. Neuron 59:648–661
Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J (2010) Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc Natl Acad Sci 107:3228–3233
Bambini-Junior V, Rodrigues L, Behr GA, Moreira JCF, Riesgo R, Gottfried C (2011) Animal model of autism induced by prenatal exposure to valproate: behavioral changes and liver parameters. Brain Res 1408:8–16
Barrett CE, Hennessey TM, Gordon KM, Ryan SJ, McNair ML, Ressler KJ, Rainnie DG (2017) Developmental disruption of amygdala transcriptome and socioemotional behavior in rats exposed to valproic acid prenatally. Mol Autism 8:42
Benchenane K, Peyrache A, Khamassi M, Tierney PL, Gioanni Y, Battaglia FP, Wiener SI (2010) Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning. Neuron 66:921–936
Bender F, Gorbati M, Cadavieco MC, Denisova N, Gao X, Holman C, Korotkova T, Ponomarenko A (2015) Theta oscillations regulate the speed of locomotion via a hippocampus to lateral septum pathway. Nat Commun 6:1–11
Beyeler A, Namburi P, Glober GF, Simonnet C, Calhoon GG, Conyers GF, Luck R, Wildes CP, Tye KM (2016) Divergent routing of positive and negative information from the amygdala during memory retrieval. Neuron 90:348–361
Brog JS, Salyapongse A, Deutch AY, Zahm DS (1993) The patterns of afferent innervation of the core and shell in the “Accumbens” part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J Comp Neurol 338:255–278
Buttelmann D, Call J, Tomasello M (2007) Behavioral cues that great apes use to forage for hidden food. Anim Cogn 11:117–128
Buzsáki G, Anastassiou CA, Koch C (2012) The origin of extracellular fields and currents—EEG, ECoG, LFP and spikes. Nat Rev Neurosci 13:407–420
Canolty RT, Knight RT (2010) The functional role of cross-frequency coupling. Trends Cogn Sci 14:506–515
Christensen J, Grønborg TK, Sørensen MJ, Schendel D, Parner ET, Pedersen LH, Vestergaard M (2013) Prenatal valproate exposure and risk of autism spectrum disorders and childhood autism. JAMA 309:1696–1703
Chrobak JJ, Buzsáki G (1996) High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci 16:3056–3066
Cohen MX, Axmacher N, Lenartz D, Elger CE, Sturm V, Schlaepfer TE (2009a) Good vibrations: cross-frequency coupling in the human nucleus accumbens during reward processing. J Cogn Neurosci 21:875–889
Cohen MX, David N, Vogeley K, Elger CE (2009b) Gamma-band activity in the human superior temporal sulcus during mentalizing from nonverbal social cues. Psychophysiology 46:43–51
Colgin LL (2013) Mechanisms and functions of theta rhythms. Annu Rev Neurosci 36:295–312
Daenen EWPM, Wolterink G, Gerrits MAFM, Van Ree JM (2002) The effects of neonatal lesions in the amygdala or ventral hippocampus on social behaviour later in life. Behav Brain Res 136:571–582
DeCoteau WE, Thorn C, Gibson DJ, Courtemanche R, Mitra P, Kubota Y, Graybiel AM (2007) Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task. Proc Natl Acad Sci 104:5644–5649
Di Ciano P, Everitt BJ (2004) Direct interactions between the basolateral amygdala and nucleus accumbens core underlie cocaine-seeking behavior by rats. J Neurosci 24:7167–7173
Donnelly NA, Holtzman T, Rich PD, Nevado-Holgado AJ, Fernando ABP, Van Dijck G, Holzhammer T, Paul O, Ruther P, Paulsen O, Robbins TW, Dalley JW (2014) Oscillatory activity in the medial prefrontal cortex and nucleus accumbens correlates with impulsivity and reward outcome tort ABL, ed. PLoS ONE 9:e111300
Favre MR, Barkat TR, Lamendola D, Khazen G, Markram H, Markram K (2013) General developmental health in the VPA-rat model of autism. Front Behav Neurosci 7:88
Fujisawa S, Buzsáki G (2011) A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities. Neuron 72:153–165
Gandal MJ, Edgar JC, Ehrlichman RS, Mehta M, Roberts TPL, Siegel SJ (2010) Validating γ oscillations and delayed auditory responses as translational biomarkers of autism. Biol Psychiatry 68:1100–1106
Goodell DJ, Ahern MA, Baynard J, Wall VL, Bland ST (2017) A novel escapable social interaction test reveals that social behavior and mPFC activation during an escapable social encounter are altered by post-weaning social isolation and are dependent on the aggressiveness of the stimulus rat. Behav Brain Res 317:1–15
Gourley SL, Taylor JR (2016) Going and stopping: dichotomies in behavioral control by the prefrontal cortex. Nat Neurosci 19:656–664
Grosenick L, Marshel JH, Deisseroth K (2015) Closed-loop and activity-guided optogenetic control. Neuron 86:106–139
Gunaydin LA, Grosenick L, Finkelstein JCC, Kauvar IV, Fenno LEE, Adhikari A, Lammel S, Mirzabekov JJJ, Airan RDD, Zalocusky KA, Tye KMM, Anikeeva P, Malenka RCC, Deisseroth K (2014) Natural neural projection dynamics underlying social behavior. Cell 157:1535–1551
Headley DB, Paré D (2013) In sync: gamma oscillations and emotional memory. Front Behav Neurosci 7:170
Hill DS, Cabrera R, Wallis Schultz D, Zhu H, Lu W, Finnell RH, Wlodarczyk BJ (2015) Autism-like behavior and epigenetic changes associated with autism as consequences of in utero exposure to environmental pollutants in a mouse model. Behav Neurol 2015:1–10
Holtzman JD (2006) Food and memory. Annu Rev Anthropol 35:361–378
Hutcheon B, Yarom Y (2000) Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci 23:216–222
Hyman JM (2010) Working memory performance correlates with prefrontal-hippocampal theta interactions but not with prefrontal neuron firing rates. Front Integr Neurosci 10:2
Itskov V, Pastalkova E, Mizuseki K, Buzsaki G, Harris KD (2008) Theta-mediated dynamics of spatial information in hippocampus. J Neurosci 28:5959–5964
Jones MW, Wilson MA (2005) Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol 3:e402
Karalis N, Dejean C, Chaudun F, Khoder S, Rozeske R, Wurtz H, Bagur S, Benchenane K, Sirota A, Courtin J, Herry C (2016) 4-Hz oscillations synchronize prefrontal-amygdala circuits during fear behavior. Nat Neurosci 19:605–612
Kay LM (2005) Theta oscillations and sensorimotor performance. Proc Natl Acad Sci 102:3863–3868
Kilias A, Canales A, Froriep UP, Park S, Egert U, Anikeeva P (2018) Optogenetic entrainment of neural oscillations with hybrid fiber probes. J Neural Eng 15:056006
Kim J, Delcasso S, Lee I (2011a) Neural correlates of object-in-place learning in hippocampus and prefrontal cortex. J Neurosci 31:16991–17006
Kim KC, Kim P, Go HS, Choi CS, Il YS, Cheong JH, Shin CY, Ko KH (2011b) The critical period of valproate exposure to induce autistic symptoms in Sprague–Dawley rats. Toxicol Lett 201:137–142
Lega B, Burke J, Jacobs J, Kahana MJ (2016) Slow-theta-to-gamma phase-amplitude coupling in human hippocampus supports the formation of new episodic memories. Cereb Cortex 26:268–278
Lesting J, Narayanan RT, Kluge C, Sangha S, Seidenbecher T, Pape HC (2011) Patterns of coupled theta activity in amygdala-hippocampal-prefrontal cortical circuits during fear extinction. PLoS One 6
Li JY, Kuo TBJ, Hsieh IT, Yang CCH (2012) Changes in hippocampal theta rhythm and their correlations with speed during different phases of voluntary wheel running in rats. Neuroscience 28:54–61
Lin H-CC, Gean P-WW, Wang C-CC, Chan Y-HH, Chen PS (2013) The amygdala excitatory/inhibitory balance in a valproate-induced rat autism model. PLoS ONE 8:e55248
Luongo FJ, Horn ME, Sohal VS (2016) Putative microcircuit-level substrates for attention are disrupted in mouse models of autism. Biol Psychiatry 79:667–675
Madsen TE, Rainnie DG (2012) Local field potentials in the rat basolateral amygdala and medial prefrontal cortex show coherent oscillations in multiple frequency bands during fear. In: Annual meeting of the society for neuroscience. Chicago
Malhotra S, Cross RW, Zhang A, van der Meer MAA (2015) Ventral striatal gamma oscillations are highly variable from trial to trial, and are dominated by behavioural state, and only weakly influenced by outcome value. Eur J Neurosci 42:2818–2832
Markram K, Rinaldi T, La MD, Sandi C, Markram H (2008) Abnormal fear conditioning and amygdala processing in an animal model of autism. Neuropsychopharmacology 33:901–912
Martin L, Iceberg E (2015) Quantifying social motivation in mice using operant conditioning. J Vis Exp e53009
Mcdonald AJ (1991) Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neuroscience 44:15–33
McGinty VB, Lardeux S, Taha SA, Kim JJ, Nicola SM (2013) Invigoration of reward seeking by cue and proximity encoding in the nucleus accumbens. Neuron 78:910–922
Meaney MJ, Dodge AM, Beatty WW (1981) Sex-dependent effects of amygdaloid lesions on the social play of prepubertal rats. Physiol Behav 26:467–472
Mizuseki K, Sirota A, Pastalkova E, Buzsáki G (2009) Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 64:267–280
Namburi P, Beyeler A, Yorozu S, Calhoon GG, Halbert SA, Wichmann R, Holden SS, Mertens KL, Anahtar M, Felix-Ortiz AC, Wickersham IR, Gray JM, Tye KM (2015) A circuit mechanism for differentiating positive and negative associations. Nature 520:675–678
O’Connor EC, Kremer Y, Lefort S, Harada M, Pascoli V, Rohner C, Lüscher C (2015) Accumbal D1R neurons projecting to lateral hypothalamus authorize feeding. Neuron 88:553–564
O’Neill P-K, Gordon JA, Sigurdsson T (2013) Theta oscillations in the medial prefrontal cortex are modulated by spatial working memory and synchronize with the hippocampus through its ventral subregion. J Neurosci 33:14211–14224
Okuyama T, Kitamura T, Roy DS, Itohara S, Tonegawa S (2016) Ventral CA1 neurons store social memory. Science 353:1536–1541
Oostenveld R, Fries P, Maris E, Schoffelen J-M (2011) FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:156869
Paxinos G, Watson C (2013) The rat brain in stereotaxic coordinates. Elsevier Science, New York, NY
Pickett CL, Gardner WL, Knowles M (2004) Getting a cue: the need to belong and enhanced sensitivity to social cues. Pers Soc Psychol Bull 30:1095–1107
Popescu AT, Popa D, Paré D (2009) Coherent gamma oscillations couple the amygdala and striatum during learning. Nat Neurosci 12:801–807
Rodier PM, Hyman SL (1998) Early environmental factors in autism. Ment Retard Dev Disabil Res Rev 4:121–128
Roullet FI, Wollaston L, deCatanzaro D, Foster JA (2010) Behavioral and molecular changes in the mouse in response to prenatal exposure to the anti-epileptic drug valproic acid. Neuroscience 170:514–522
Roullet FI, Lai JKY, Foster JA (2013) In utero exposure to valproic acid and autism—a current review of clinical and animal studies. Neurotoxicol Teratol 36:47–56
Schneider T, Przewłocki R (2005) Behavioral alterations in rats prenatally exposed to valproic acid: animal model of autism. Neuropsychopharmacology 30:80–89
Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275:1593–1599
Stuber GD, Sparta DR, Stamatakis AM, van Leeuwen WA, Hardjoprajitno JE, Cho S, Tye KM, Kempadoo KA, Zhang F, Deisseroth K, Bonci A (2011) Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475:377–380
Stujenske JM, Likhtik E, Topiwala MA, Gordon JA (2014) Fear and safety engage competing patterns of theta-gamma coupling in the basolateral amygdala. Neuron 83:919–933
Taha SA, Fields HL (2006) Inhibitions of nucleus accumbens neurons encode a gating signal for reward-directed behavior. J Neurosci 26:217–222
Tendler A, Wagner S (2015) Different types of theta rhythmicity are induced by social and fearful stimuli in a network associated with social memory. Elife 2015:1–22
Terada S, Takahashi S, Sakurai Y (2013) Oscillatory interaction between amygdala and hippocampus coordinates behavioral modulation based on reward expectation. Front Behav Neurosci 7:177
Tort ABL, Komorowski R, Eichenbaum H, Kopell N (2010) Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. J Neurophysiol 104:1195–1210
Tyzio R, Nardou R, Ferrari DC, Tsintsadze T, Shahrokhi A, Eftekhari S, Khalilov I, Tsintsadze V, Brouchoud C, Chazal G, Lemonnier E, Lozovaya N, Burnashev N, Ben-Ari Y (2014) Oxytocin-mediated GABA inhibition during delivery attenuates autism pathogenesis in rodent offspring. Science 343:675–679
van Kerkhof LWM, Trezza V, Mulder T, Gao P, Voorn P, Vanderschuren LJMJ (2013) Cellular activation in limbic brain systems during social play behaviour in rats. Brain Struct Funct 219:1181–1211
Wiggert N, Wilhelm FH, Boger S, Georgii C, Klimesch W, Blechert J (2017) Social pavlovian conditioning: short- and long-term effects and the role of anxiety and depressive symptoms. Soc Cogn Affect Neurosci 12:329–339
Wolterink G, Daenen LEWPM, Dubbeldam S, Gerrits MAFM, Van Rijn R, Kruse CG, Van Der Heijden JAM, Van Ree JM (2001) Early amygdala damage in the rat as a model for neurodevelopmental psychopathological disorders. Eur Neuropsychopharmacol 11:51–59
Acknowledgements
This work was supported by NIH P50 MH100023 and R01 DA044297. The Yerkes National Primate Research Center is supported by the Office of Research Infrastructure Programs/OD P51 OD011132.
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Hsu, CC., Madsen, T.E., O’Gorman, E. et al. Reward-related dynamical coupling between basolateral amygdala and nucleus accumbens. Brain Struct Funct 225, 1873–1888 (2020). https://doi.org/10.1007/s00429-020-02099-2
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DOI: https://doi.org/10.1007/s00429-020-02099-2