Stimulus‑seeking in rats is accompanied by increased c‑Fos expression in hippocampal CA1 as well as short 22 kHz and flat 50 kHz calls

• Autorzy: Robakiewicz I. , Polak M. , Rawska M. , Alberski D. , Polowy R. , Wytrychiewicz K. , Syperek M. , Matysiak J. , Filipkowski R.K.
• Języki publikacji: EN

Abstrakty

EN

We determined CA1 hippocampal field to be involved in self‑exposure, a type of novelty‑seeking behaviour that has also been associated with short 22 kHz and flat 50 kHz ultrasonic vocalizations (USV) in adult male Long‑Evans rats. Rats were habituated for three days to a self‑exposure cage with two nose‑poke holes. On day four, the animals from the experimental group were allowed to turn the cage light off for 5 s with a nose‑poke (test/self‑exposure session), while rats from control‑yoked group had changing light conditions coupled and identical to the experimental animals. The experimental rats performed more nose‑pokes during self‑exposure session than animals from the control group. This effect was accompanied by a higher density of c‑Fos‑positive nuclei in the hippocampal CA1. There were no significant group differences in c‑Fos expression in other brain regions analysed. However, possible involvement of several other structures in self‑exposure (i.e., CA3, the dentate gyrus, amygdala, prefrontal cortex, and nucleus accumbens) is also discussed, as their correlational activity, reflected by c‑Fos immunoactivity, was observed in the experimental rats. During test sessions, there were more nose‑pokes accompanied by short 22 kHz calls and 50 kHz calls performed by the rats of the experimental group than of the control group. The CA1 region has previously been associated with novelty; short 22 kHz USV and flat 50 kHz USV could be associated with self‑exposure, also they appear to be emitted correlatively.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2019
• Tom: 79
• Numer: 3
• Opis fizyczny: p.309-317,fig.,ref.

Twórcy

autor

Robakiewicz I.

• Department of Biological Psychology, University of Economics and Human Sciences in Warsaw, Warsaw, Poland

autor

Polak M.

• Department of Biological Psychology, University of Economics and Human Sciences in Warsaw, Warsaw, Poland

autor

Rawska M.

• Department of Biological Psychology, University of Economics and Human Sciences in Warsaw, Warsaw, Poland

autor

Alberski D.

• Department of Biological Psychology, University of Economics and Human Sciences in Warsaw, Warsaw, Poland

autor

Polowy R.

• Behavior and Metabolism Research Laboratory, Mossakowski Medical Research Centre, Polish Academy of Sciences, Warsaw, Poland

autor

Wytrychiewicz K.

• Department of Biological Psychology, University of Economics and Human Sciences in Warsaw, Warsaw, Poland

autor

Syperek M.

• Department of Biological Psychology, University of Economics and Human Sciences in Warsaw, Warsaw, Poland

autor

Matysiak J.

• Department of Biological Psychology, University of Economics and Human Sciences in Warsaw, Warsaw, Poland

autor

Filipkowski R.K.

• Behavior and Metabolism Research Laboratory, Mossakowski Medical Research Centre, Polish Academy of Sciences, Warsaw, Poland

Bibliografia

• Adhikari A, Lerner TN, Finkelstein J, Pak S, Jennings JH, Davidson TJ, Ferenczi E, Gunaydin LA, Mirzabekov JJ, Ye L, Kim SY, Lei A, Deisseroth K (2015) Basomedial amygdala mediates top‑down control of anxiety and fear. Nature 527: 179–185.
• Aggleton JP, Brown MW, Albasser MM (2012) Contrasting brain activity patterns for item recognition memory and associative recognition memory: insights from immediate‑early gene functional imaging. Neuropsychologia 50: 3141–3155.
• Albasser MM, Chapman RJ, Amin E, Iordanova MD, Vann SD, Aggleton JP (2010) New behavioral protocols to extend our knowledge of rodent object recognition memory. Learn Mem 17: 407–419.
• Arruda‑Carvalho M, Clem RL (2014) Pathway‑selective adjustment of prefrontal‑amygdala transmission during fear encoding. J  Neurosci 34: 15601–15609.
• Arruda‑Carvalho  M, Clem RL (2015) Prefrontal‑amygdala fear networks come into focus. Front Syst Neurosci 9: 145.
• Balleine BW (2005) Neural bases of food‑seeking: affect, arousal and reward in corticostriatolimbic circuits. Physiol Behav 86: 717–730.
• Barker DJ, Root DH, Ma S, Jha S, Megehee L, Pawlak AP, West MO (2010) Dose‑dependent differences in short ultrasonic vocalizations emitted by rats during cocaine self‑administration. Psychopharmacology 211: 435–442.
• Barker DJ, Simmons SJ, Servilio LC, Bercovicz D, Ma S, Root DH, Pawlak AP, West MO (2014) Ultrasonic vocalizations: evidence for an affective opponent process during cocaine self‑administration. Psychopharmacology 231: 909–918.
• Barker DJ, Simmons SJ, West MO (2015) Ultrasonic vocalizations as a measure of affect in preclinical models of drug abuse: a review of current findings. Curr Neuropharmacol 13: 193–210.
• Bialy M, Bogacki‑Rychlik W, Kasarello K, Nikolaev E, Sajdel‑Sulkowska EM (2016) Modulation of 22‑kHz postejaculatory vocalizations by conditioning to new place: Evidence for expression of a positive emotional state. Behav Neurosci 130: 415–421.
• Bieri KW, Bobbitt KN, Colgin LL (2014) Slow and fast gamma rhythms coordinate different spatial coding modes in hippocampal place cells. Neuron 82: 670–681.
• Bourgeois JP, Meas‑Yeadid  V, Lesourd AM, Faure P, Pons S, Maskos U, Changeux JP, Olivo‑Marin JC, Granon S (2012) Modulation of the mouse prefrontal cortex activation by neuronal nicotinic receptors during novelty exploration but not by exploration of a familiar environment. Cereb Cortex 22: 1007–1015.
• Britt JP, Benaliouad F, McDevitt RA, Stuber GD, Wise RA, Bonci A (2012) Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens. Neuron 76: 790–803. Brudzynski SM, Bihari F, Ociepa D, Fu XW (1993) Analysis of 22 kHz ultrasonic vocalization in laboratory rats: long and short calls. Physiol Behav 54: 215–221.
• Brudzynski SM (2007) Ultrasonic calls of rats as indicator variables of negative or positive states: acetylcholine‑dopamine interaction and acoustic coding. Behav Brain Res 182: 261–273.
• Brudzynski SM (2013) Ethotransmission: communication of emotional states through ultrasonic vocalization in rats. Curr Opin Neurobiol 23: 310–317.
• Brudzynski SM (2015) Pharmacology of ultrasonic vocalizations in adult rats: significance, call classification and neural substrate. Curr Neuropharmacol 13: 180–192.
• Burgdorf J, Kroes RA, Moskal JR, Pfaus JG, Brudzynski SM, Panksepp J (2008) Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: Behavioral concomitants, relationship to reward, and self‑administration of playback. J Comp Psychol 122: 357–367.
• Burgdorf J, Panksepp J, Moskal JR (2011) Frequency‑modulated 50 kHz ultrasonic vocalizations: a tool for uncovering the molecular substrates of positive affect. Neurosci Biobehav Rev 35: 1831–1836.
• Comba R, Gervais N, Mumby D, Holahan M (2015) Emergence of spatial behavioral function and associated mossy fiber connectivity and c‑Fos labeling patterns in the hippocampus of rats. F1000Res 4: 396.
• Cui Q, Li Q, Geng H, Chen L, Ip NY, Ke Y, Yung WH (2018) Dopamine receptors mediate strategy abandoning via modulation of a specific prelimbic cortex‑nucleus accumbens pathway in mice. Proc Natl Acad Sci 115: E4890–E4899.
• Ding DC, Gabbott PL, Totterdell S (2001) Differences in the laminar origin of projections from the medial prefrontal cortex to the nucleus accumbens shell and core regions in the rat. Brain Res 917: 81–89.
• Duszkiewicz AJ, McNamara CG, Takeuchi T, Genzel L (2019) Novelty and dopaminergic modulation of memory persistence: a tale of two systems. Trends Neurosci 42: 102–114.
• Duvelle E, Grieves RM, Hok V, Poucet B, Arleo A, Jeffery K, Save E (2019) Insensitivity of place cells to the value of spatial goals in a two‑choice flexible navigation task. J Neurosci 39: 2522–2541.
• Eichenbaum H, Yonelinas AP, Ranganath C (2007) The medial temporal lobe and recognition memory. Annu Rev Neurosci 30: 123–152.
• Farley D, Matysiak J (2008) The effect of stressor level grading on the stimulus seeking behavior of rats differing in emotional reactivity. Polish Psychological Bulletin 39: 98–103.
• Filipkowski RK, Rydz M, Berdel B, Morys J, Kaczmarek L (2000) Tactile experience induces c‑fos expression in rat barrel cortex. Learn Mem 7: 116–122.
• Filipkowski RK, Rydz  M, Kaczmarek  L (2001) Expression of c‑Fos, Fos B, Jun B, and Zif268 transcription factor proteins in rat barrel cortex following apomorphine‑evoked whisking behavior. Neuroscience 106: 679–688.
• Gabbott PL, Warner TA, Jays PR, Salway P, Busby SJ (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492: 145–177.
• Groenewegen HJ, Galis‑de Graaf Y, Smeets WJ (1999) Integration and segregation of limbic cortico‑striatal loops at the thalamic level: an experimental tracing study in rats. J Chem Neuroanat 16: 167–185.
• Handa RJ, Nunley KM, Bollnow MR (1993) Induction of c‑fos mRNA in the brain and anterior pituitary gland by a novel environment. Neuroreport 4: 1079–1082.
• Hart G, Leung BK, Balleine BW (2014) Dorsal and ventral streams: the distinct role of striatal subregions in the acquisition and performance of goal‑directed actions. Neurobiol Learn Mem 108: 104–118.
• Hess US, Lynch G, Gall CM (1995) Regional patterns of c‑fos mRNA expression in rat hippocampus following exploration of a novel environment versus performance of a  well‑learned discrimination. J  Neurosci 15: 7796–7809.
• Hoang TH, Aliane V, Manahan‑Vaughan D (2018) Novel encoding and updating of positional, or directional, spatial cues are processed by distinct hippocampal subfields: Evidence for parallel information processing and the “what” stream. Hippocampus 28: 315–326.
• Jaeger BN, Linker SB, Parylak SL, Barron JJ, Gallina IS, Saavedra CD, Fitzpatrick C, Lim CK, Schafer ST, Lacar B, Jessberger S, Gage FH (2018) A novel environment‑evoked transcriptional signature predicts reactivity in single dentate granule neurons. Nat Commun 9: 3084.
• Jaworski J, Biedermann IW, Lapinska J, Szklarczyk A, Figiel I, Konopka D, Nowicka D, Filipkowski RK, Hetman M, Kowalczyk A, Kaczmarek L (1999) Neuronal excitation‑driven and AP‑1‑dependent activation of tissue inhibitor of metalloproteinases‑1 gene expression in rodent hippocampus. J Biol Chem 274: 28106–28112.
• Jaworski J, Kalita K, Knapska E (2018) c‑Fos and neuronal plasticity: the aftermath of Kaczmarek’s theory. Acta Neurobiol Exp 78: 287–296.
• Jenkins TA, Amin E, Pearce JM, Brown MW, Aggleton JP (2004) Novel spatial arrangements of familiar visual stimuli promote activity in the rat hippocampal formation but not the parahippocampal cortices: a c‑fos expression study. Neuroscience 124: 43–52.
• Kaminska B, Filipkowski RK, Biedermann IW, Konopka D, Nowicka D, Hetman  M, Dabrowski  M, Gorecki DC, Lukasiuk K, Szklarczyk AW, Kaczmarek L (1997) Kainate‑evoked modulation of gene expression in rat brain. Acta Biochim Pol 44: 781–789.
• Kemp A, Tischmeyer  W, Manahan‑Vaughan D (2013) Learning‑facilitated long‑term depression requires activation of the immediate early gene, c‑fos, and is transcription dependent. Behav Brain Res 254: 83–91.
• Kerr JE, Beck SG, Handa RJ (1996) Androgens selectively modulate C‑fos messenger RNA induction in the rat hippocampus following novelty. Neuroscience 74: 757–766.
• Kinnavane L, Amin E, Horne M, Aggleton JP (2014) Mapping parahippocampal systems for recognition and recency memory in the absence of the rat hippocampus. Eur J Neurosci 40: 3720–3734.
• Klawonn AM, Malenka RC (2019) Nucleus accumbens modulation in reward and aversion. Cold Spring Harb Symp Quant Biol 83: 1–11.
• Knapska E, Walasek G, Nikolaev E, Neuhausser‑Wespy F, Lipp HP, Kaczmarek  L, Werka T (2006) Differential involvement of the central amygdala in appetitive versus aversive learning. Learn Mem 13: 192–200.
• Knapska E, Radwanska K, Werka T, Kaczmarek L (2007) Functional internal complexity of amygdala: focus on gene activity mapping after behavioral training and drugs of abuse. Physiol Rev 87: 1113–1173.
• Kromkhun P, Katou M, Hashimoto H, Terada M, Moon C, Saito TR (2013) Quantitative and qualitative analysis of rat pup ultrasonic vocalization sounds induced by a hypothermic stimulus. Lab Anim Res 29: 77–83.
• Larkin MC, Lykken C, Tye LD, Wickelgren JG, Frank LM (2014) Hippocampal output area CA1 broadcasts a generalized novelty signal during an object‑place recognition task. Hippocampus 24: 773–783.
• Lee M, Manders TR, Eberle SE, Su C, D’Amour J, Yang R, Lin HY, Deisseroth K, Froemke RC, Wang J (2015) Activation of corticostriatal circuitry relieves chronic neuropathic pain. J Neurosci 35: 5247–5259.
• Lever C, Burton S, Jeewajee A, Wills TJ, Cacucci F, Burgess N, O’Keefe J (2010) Environmental novelty elicits a later theta phase of firing in CA1 but not subiculum. Hippocampus 20: 229–234.
• Manahan‑Vaughan D, Braunewell KH (1999) Novelty acquisition is associated with induction of hippocampal long‑term depression. Proc Natl Acad Sci 96: 8739–8744.
• Manns JR, Zilli EA, Ong KC, Hasselmo ME, Eichenbaum H (2007) Hippocampal CA1 spiking during encoding and retrieval: relation to theta phase. Neurobiol Learn Mem 87: 9–20.
• Martinez E, Lin HH, Zhou H, Dale J, Liu K, Wang J (2017) Corticostriatal regulation of acute pain. Front Cell Neurosci 11: 146.
• Matysiak J (1978) Exposition of visual stimuli in an aversive situation and self‑exposure to light in rats. Pavlov J Biol Sci 13: 151–153.
• Mohammed AH, Zhu SW, Darmopil S, Hjerling‑Leffler J, Ernfors P, Winblad B, Diamond MC, Eriksson PS, Bogdanovic N (2002) Environmental enrichment and the brain. Prog Brain Res 138: 109–133.
• Moser EI, Kropff E, Moser MB (2008) Place cells, grid cells, and the brain’s spatial representation system. Annu Rev Neurosci 31: 69–89.
• Mulvihill KG, Brudzynski SM (2018) Non‑pharmacological induction of rat 50kHz ultrasonic vocalization: Social and non‑social contexts differentially induce 50 kHz call subtypes. Physiol Behav 196: 200–207.
• Mun HS, Saab BJ, Ng E, McGirr A, Lipina TV, Gondo Y, Georgiou J, Roder JC (2015) Self‑directed exploration provides a  Ncs1‑dependent learning bonus. Sci Rep 5: 17697.
• Murugan  M, Jang HJ, Park  M, Miller EM, Cox J, Taliaferro JP, Parker NF, Bhave V, Hur H, Liang Y, Nectow AR, Pillow JW, Witten IB (2017) Combined social and spatial coding in a descending projection from the prefrontal cortex. Cell 171: 1663–1677.
• Nikolaev E, Werka T, Kaczmarek L (1992) C‑fos protooncogene expression in rat brain after long‑term training of two‑way active avoidance reaction. Behav Brain Res 48: 91–94.
• O’Donnell P, Lavin A, Enquist LW, Grace AA, Card JP (1997) Interconnected parallel circuits between rat nucleus accumbens and thalamus revealed by retrograde transynaptic transport of pseudorabies virus. J Neurosci 17: 2143–2167.
• Osinski J, Matysiak J (2008) The effects of handling on the exploratory activity of rats in settings varying in level of sensory stimulation. Polish Psychological Bulletin 39: 89–97.
• Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th edition, Academic Press. Penley SC, Hinman JR, Long LL, Markus EJ, Escabi MA, Chrobak JJ (2013) Novel space alters theta and gamma synchrony across the longitudinal axis of the hippocampus. Front Syst Neurosci 7: 20. Petrovich GD, Risold PY, Swanson LW (1996) Organization of projections from the basomedial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 374: 387–420.
• Portfors CV (2007) Types and functions of ultrasonic vocalizations in laboratory rats and mice. J Am Assoc Lab Anim Sci 46: 28–34.
• Schwarting RK, Jegan N, Wohr M (2007) Situational factors, conditions and individual variables which can determine ultrasonic vocalizations in male adult Wistar rats. Behav Brain Res 182: 208–222.
• Selleck RA, Zhang W, Samberg HD, Padival M, Rosenkranz JA (2018) Limited prefrontal cortical regulation over the basolateral amygdala in adolescent rats. Sci Rep 8: 17171.
• Sesack SR, Deutch AY, Roth RH, Bunney BS (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract‑tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290: 213–242.
• Sheth A, Berretta S, Lange N, Eichenbaum H (2008) The amygdala modulates neuronal activation in the hippocampus in response to spatial novelty. Hippocampus 18: 169–181.
• Simola N (2015) Rat ultrasonic vocalizations and behavioral neuropharmacology: from the screening of drugs to the study of disease. Curr Neuropharmacol 13: 164–179.
• Simola N, Costa G (2018) Emission of categorized 50‑kHz ultrasonic vocalizations in rats repeatedly treated with amphetamine or apomorphine: Possible relevance to drug‑induced modifications in the emotional state. Behav Brain Res 347: 88–98.
• Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99: 195–231.
• Stefanik MT, Kupchik YM, Kalivas PW (2016) Optogenetic inhibition of cortical afferents in the nucleus accumbens simultaneously prevents cue‑induced transient synaptic potentiation and cocaine‑seeking behavior. Brain Struct Funct 221: 1681–1689.
• Stopper CM, Floresco SB (2011) Contributions of the nucleus accumbens and its subregions to different aspects of risk‑based decision making. Cogn Affect Behav Neurosci 11: 97–112.
• Tanimizu T, Kono K, Kida S (2018) Brain networks activated to form object recognition memory. Brain Res Bull 141: 27–34.
• Turner CA, Yang MC, Lewis MH (2002) Environmental enrichment: effects on stereotyped behavior and regional neuronal metabolic activity. Brain Res 938: 15–21.
• Valenti O, Mikus N, Klausberger T (2018) The cognitive nuances of surprising events: exposure to unexpected stimuli elicits firing variations in neurons of the dorsal CA1 hippocampus. Brain Struct Funct 223: 3183–3211.
• Van Elzakker M, Fevurly RD, Breindel T, Spencer RL (2008) Environmental novelty is associated with a selective increase in Fos expression in the output elements of the hippocampal formation and the perirhinal cortex. Learn Mem 15: 899–908.
• Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51: 32–58.
• Walton ME, Bannerman DM, Rushworth MF (2002) The role of rat medial frontal cortex in effort‑based decision making. J  Neurosci 22: 10996–11003.
• Wan H, Aggleton JP, Brown MW (1999) Different contributions of the hippocampus and perirhinal cortex to recognition memory. J Neurosci 19: 1142–1148.
• Willadsen  M, Best LM, Wohr  M, Clarke PBS (2018) Effects of anxiogenic drugs on the emission of 22‑ and 50‑kHz ultrasonic vocalizations in adult rats. Psychopharmacology 235: 2435–2445.
• Winters BD, Saksida LM, Bussey TJ (2008) Object recognition memory: neurobiological mechanisms of encoding, consolidation and retrieval. Neurosci Biobehav Rev 32: 1055–1070. Wohr M, Houx B, Schwarting RK, Spruijt B (2008) Effects of experience and context on 50‑kHz vocalizations in rats. Physiol Behav 93: 766–776.
• Wright JM, Gourdon JC, Clarke PB (2010) Identification of multiple call categories within the rich repertoire of adult rat 50‑kHz ultrasonic vocalizations: effects of amphetamine and social context. Psychopharmacology 211: 1–13.
• Wright JM, Dobosiewicz MR, Clarke PB (2012) alpha‑ and beta‑Adrenergic receptors differentially modulate the emission of spontaneous and amphetamine‑induced 50‑kHz ultrasonic vocalizations in adult rats. Neuropsychopharmacology 37: 808–821.
• Xu H, Baracskay P, O’Neill J, Csicsvari J (2019) Assembly responses of hippocampal CA1 place cells predict learned behavior in goal‑directed spatial tasks on the radial eight‑arm maze. Neuron 101: 119–132.
• Zheng C, Bieri KW, Hwaun E, Colgin LL (2016) Fast gamma rhythms in the hippocampus promote encoding of novel object‑place pairings. eNeuro 3: 1–19.
• Zhou H, Martinez E, Lin HH, Yang R, Dale JA, Liu K, Huang D, Wang J (2018) Inhibition of the prefrontal projection to the nucleus accumbens enhances pain sensitivity and affect. Front Cell Neurosci 12: 240.
• Zhu XO, Brown MW, McCabe BJ, Aggleton JP (1995) Effects of the novelty or familiarity of visual stimuli on the expression of the immediate early gene c‑fos in rat brain. Neuroscience 69: 821–829.
• Zhu XO, McCabe BJ, Aggleton JP, Brown MW (1996) Mapping visual recognition memory through expression of the immediate early gene c‑fos. Neuroreport 7: 1871–1875.

Identyfikatory

DOI

10.21307/ane‑2019‑029