Top

Published in:

01-05-2018 | Original Article

Comparing brain activity patterns during spontaneous exploratory and cue-instructed learning using single photon-emission computed tomography (SPECT) imaging of regional cerebral blood flow in freely behaving rats

Authors: A. Mannewitz, J. Bock, S. Kreitz, A. Hess, J. Goldschmidt, H. Scheich, Katharina Braun

Published in: Brain Structure and Function | Issue 4/2018

Abstract

Learning can be categorized into cue-instructed and spontaneous learning types; however, so far, there is no detailed comparative analysis of specific brain pathways involved in these learning types. The aim of this study was to compare brain activity patterns during these learning tasks using the in vivo imaging technique of single photon-emission computed tomography (SPECT) of regional cerebral blood flow (rCBF). During spontaneous exploratory learning, higher levels of rCBF compared to cue-instructed learning were observed in motor control regions, including specific subregions of the motor cortex and the striatum, as well as in regions of sensory pathways including olfactory, somatosensory, and visual modalities. In addition, elevated activity was found in limbic areas, including specific subregions of the hippocampal formation, the amygdala, and the insula. The main difference between the two learning paradigms analyzed in this study was the higher rCBF observed in prefrontal cortical regions during cue-instructed learning when compared to spontaneous learning. Higher rCBF during cue-instructed learning was also observed in the anterior insular cortex and in limbic areas, including the ectorhinal and entorhinal cortexes, subregions of the hippocampus, subnuclei of the amygdala, and the septum. Many of the rCBF changes showed hemispheric lateralization. Taken together, our study is the first to compare partly lateralized brain activity patterns during two different types of learning.

Alvarez EO, Banzan AM (2011) Functional lateralization of the baso-lateral amygdala neural circuits modulating the motivated exploratory behaviour in rats: role of histamine. Behav Brain Res 218(1):158–164. https://doi.org/10.1016/j.bbr.2010.11.024 PubMedCrossRef

Andersen RA, Snyder LH, Bradley DC, Xing J (1997) Multimodal representation of space in the posterior parietal cortex and its use in planning movements. Annu Rev Neurosci 20:303–330. https://doi.org/10.1146/annurev.neuro.20.1.303 PubMedCrossRef

Baker KB, Kim JJ (2004) Amygdalar lateralization in fear conditioning: evidence for greater involvement of the right amygdala. Behav Neurosci 118(1):15–23. https://doi.org/10.1037/0735-7044.118.1.15 PubMedCrossRef

Bandler R, Shipley MT (1994) Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? Trends Neurosci 17(9):379–389PubMedCrossRef

Bhattacharya S, Herrera-Molina R, Sabanov V, Ahmed T, Iscru E, Stober F, Richter K, Fischer KD, Angenstein F, Goldschmidt J, Beesley PW, Balschun D, Smalla KH, Gundelfinger ED, Montag D (2017) Genetically induced retrograde amnesia of associative memories after neuroplastin ablation. Biol Psychiatry 81(2):124–135. https://doi.org/10.1016/j.biopsych.2016.03.2107 PubMedCrossRef

Botvinick M, Plaut DC (2002) Representing task context: proposals based on a connectionist model of action. Psychol Res 66(4):298–311. https://doi.org/10.1007/s00426-002-0103-8 PubMedCrossRef

Brito GN, Brito LS (1990) Septohippocampal system and the prelimbic sector of frontal cortex: a neuropsychological battery analysis in the rat. Behav Brain Res 36(1–2):127–146PubMedCrossRef

Brown MW, Aggleton JP (2001) Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2(1):51–61. https://doi.org/10.1038/35049064 PubMedCrossRef

Brunjes PC, Illig KR, Meyer EA (2005) A field guide to the anterior olfactory nucleus (cortex). Brain Res Brain Res Rev 50(2):305–335. https://doi.org/10.1016/j.brainresrev.2005.08.005 PubMedCrossRef

Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35(4):625–641PubMedCrossRef

Burwell RD, Amaral DG (1998a) Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. J Comp Neurol 398(2):179–205PubMedCrossRef

Burwell RD, Amaral DG (1998b) Perirhinal and postrhinal cortices of the rat: interconnectivity and connections with the entorhinal cortex. J Comp Neurol 391(3):293–321PubMedCrossRef

Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4(6):215–222PubMedCrossRef

Chen LL, Lin LH, Green EJ, Barnes CA, McNaughton BL (1994) Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Exp Brain Res 101(1):8–23PubMedCrossRef

Choi DC, Maguschak KA, Ye K, Jang SW, Myers KM, Ressler KJ (2010) Prelimbic cortical BDNF is required for memory of learned fear but not extinction or innate fear. Proc Natl Acad Sci U S A 107(6):2675–2680. https://doi.org/10.1073/pnas.0909359107 PubMedPubMedCentralCrossRef

Coleman-Mesches K, McGaugh JL (1995) Differential involvement of the right and left amygdalae in expression of memory for aversively motivated training. Brain Res 670(1):75–81PubMedCrossRef

Concha ML, Bianco IH, Wilson SW (2012) Encoding asymmetry within neural circuits. Nat Rev Neurosci 13(12):832–843. https://doi.org/10.1038/nrn3371 PubMedCrossRef

Corwin J, Reep R (1998) Rodent posterior parietal cortex as a component of a cortical network mediating directed spatial attention. Psychobiology 26:87–102

Czajkowski R, Jayaprakash B, Wiltgen B, Rogerson T, Guzman-Karlsson MC, Barth AL, Trachtenberg JT, Silva AJ (2014) Encoding and storage of spatial information in the retrosplenial cortex. Proc Natl Acad Sci USA 111(23):8661–8666. https://doi.org/10.1073/pnas.1313222111 PubMedPubMedCentralCrossRef

Davis M (1992) The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15:353–375PubMedCrossRef

Deacon TW, Eichenbaum H, Rosenberg P, Eckmann KW (1983) Afferent connections of the perirhinal cortex in the rat. J Comp Neurol 220(2):168–190PubMedCrossRef

Denenberg VH (1981) Hemispheric laterality in animals and the effects of early experience. Behav Brain Sci 4(1):1–21. https://doi.org/10.1017/S0140525X00007330 CrossRef

Denenberg VH, Garbanati J, Sherman DA, Yutzey DA, Kaplan R (1978) Infantile stimulation induces brain lateralization in rats. Science 201(4361):1150–1152PubMedCrossRef

Doeller CF, King JA, Burgess N (2008) Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory. Proc Natl Acad Sci USA 105(15):5915–5920. https://doi.org/10.1073/pnas.0801489105 PubMedPubMedCentralCrossRef

Duncan GH, Albanese MC (2003) Is there a role for the parietal lobes in the perception of pain? Adv Neurol 93:69–86PubMed

Dyck M, Loughead J, Kellermann T, Boers F, Gur RC, Mathiak K (2011) Cognitive versus automatic mechanisms of mood induction differentially activate left and right amygdala. Neuroimage 54(3):2503–2513. https://doi.org/10.1016/j.neuroimage.2010.10.013 PubMedCrossRef

Endepols H, Sommer S, Backes H, Wiedermann D, Graf R, Hauber W (2010) Effort-Based Decision Making in the rat: an [18F] fluorodeoxyglucose micro positron emission tomography study. J Neurosci 30(29):9708–9714PubMedCrossRef

Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15(2):85–93. https://doi.org/10.1016/j.tics.2010.11.004 PubMedCrossRef

Fanselow MS, Gale GD (2003) The amygdala, fear, and memory. Ann N Y Acad Sci 985:125–134PubMedCrossRef

Fujiwara J, Tobler PN, Taira M, Iijima T, Tsutsui K (2009) Segregated and integrated coding of reward and punishment in the cingulate cortex. J Neurophysiol 101(6):3284–3293. https://doi.org/10.1152/jn.90909.2008 PubMedCrossRef

Fyhn M, Molden S, Witter MP, Moser EI, Moser MB (2004) Spatial representation in the entorhinal cortex. Science 305(5688):1258–1264. https://doi.org/10.1126/science.1099901 PubMedCrossRef

Gianaros PJ, Derbyshire SW, May JC, Siegle GJ, Gamalo MA, Jennings JR (2005) Anterior cingulate activity correlates with blood pressure during stress. Psychophysiology 42(6):627–635. https://doi.org/10.1111/j.1469-8986.2005.00366.x PubMedPubMedCentralCrossRef

Giovannini MG, Rakovska A, Benton RS, Pazzagli M, Bianchi L, Pepeu G (2001) Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience 106(1):43–53PubMedCrossRef

Goldschmidt J, Wanger T, Engelhorn A, Friedrich H, Happel M, Ilango A, Engelmann M, Stuermer IW, Ohl FW, Scheich H (2010) High-resolution mapping of neuronal activity using the lipophilic thallium chelate complex TlDDC: protocol and validation of the method. Neuroimage 49(1):303–315. https://doi.org/10.1016/j.neuroimage.2009.08.012 PubMedCrossRef

Gorges M, Roselli F, Müller HP, Ludolph AC, Rasche V, Kassubek J. Functional connectivity mapping in the animal model: principles and applications of resting-state fMRI. Front Neurol 2017 May 10;8:200. https://doi.org/10.3389/fneur.2017.00200. (eCollection 2017. Review. PubMed PMID: 28539914; PubMed Central PMCID: PMC5423907)

Hellige JB (1990) Hemispheric asymmetry. Annu Rev Psychol 41:55–80. https://doi.org/10.1146/annurev.ps.41.020190.000415 PubMedCrossRef

Hellige JB (1993) Hemispheric Asymmetry: What’s Right and What’s Left. Harvard University Press, Cambridge

Hess A, Axmann R, Rech J, Finzel S, Heindl C, Kreitz S, Sergeeva M, Saake M, Garcia M, Kollias G, Straub RH, Sporns O, Doerfler A, Brune K, Schett G (2011) Blockade of TNF-α rapidly inhibits pain responses in the central nervous system. Proc Natl Acad Sci 108(9):3731–3736PubMedPubMedCentralCrossRef

Holschneider DP, Yang J, Sadler TR, Nguyen PT, Givrad TK, Maarek JM (2006) Mapping cerebral blood flow changes during auditory-cued conditioned fear in the nontethered, nonrestrained rat. Neuroimage 29(4):1344–1358. https://doi.org/10.1016/j.neuroimage.2005.08.038 PubMedCrossRef

Honey RC, Watt A, Good M (1998) Hippocampal Lesions Disrupt an Associative Mismatch Process. J Neurosci 18(6):2226–2230PubMedCrossRef

Ikemoto S (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56(1):27–78. https://doi.org/10.1016/j.brainresrev.2007.05.004 PubMedPubMedCentralCrossRef

Kennerley SW, Walton ME, Behrens TE, Buckley MJ, Rushworth MF (2006) Optimal decision making and the anterior cingulate cortex. Nat Neurosci 9(7):940–947. https://doi.org/10.1038/nn1724 PubMedCrossRef

Kim JJ, Jung MW (2006) Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review. Neurosci Biobehav Rev 30(2):188–202. https://doi.org/10.1016/j.neubiorev.2005.06.005 PubMedCrossRef

Knabl J, Witschi R, Hösl K, Reinold H, Zeilhofer UB, Ahmadi S, Brockhaus J, Sergejeva M, Hess A, Brune K, Fritschy J-M, Rudolph U, Möhler H, Zeilhofer HU (2008) Reversal of pathological pain through specific spinal GABAA receptor subtypes. Nature 451(7176):330–334PubMedCrossRef

Knight R (1996) Contribution of human hippocampal region to novelty detection. Nature 383(6597):256–259. https://doi.org/10.1038/383256a0 PubMedCrossRef

Knight DC, Smith CN, Cheng DT, Stein EA, Helmstetter FJ (2004) Amygdala and hippocampal activity during acquisition and extinction of human fear conditioning. Cogn Affect Behav Neurosci 4(3):317–325PubMedCrossRef

Kolb B, Sutherland RJ, Nonneman AJ, Whishaw IQ (1982) Asymmetry in the cerebral hemispheres of the rat, mouse, rabbit, and cat: the right hemisphere is larger. Exp Neurol 78(2):348–359PubMedCrossRef

Kolb B, Buhrmann K, McDonald R, Sutherland RJ (1994) Dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial navigation and recognition memory in the rat. Cereb Cortex 4(6):664–680PubMedCrossRef

Kolodziej A, Lippert M, Angenstein F, Neubert J, Pethe A, Grosser OS, Amthauer H, Schroeder UH, Reymann KG, Scheich H, Ohl FW, Goldschmidt J (2014) SPECT-imaging of activity-dependent changes in regional cerebral blood flow induced by electrical and optogenetic self-stimulation in mice. Neuroimage 103:171–180. https://doi.org/10.1016/j.neuroimage.2014.09.023 PubMedCrossRef

Koob GF, Riley SJ, Smith SC, Robbins TW (1978) Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi and olfactory tubercle on feeding, locomotor activity, and amphetamine anorexia in the rat. J Comp Physiol Psychol 92(5):917–927PubMedCrossRef

LaBar KS, Gatenby JC, Gore JC, LeDoux JE, Phelps EA (1998) Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 20(5):937–945PubMedCrossRef

Ledoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184PubMedCrossRef

Leon MI, Poytress BS, Weinberger NM (2008) Avoidance learning facilitates temporal processing in the primary auditory cortex. Neurobiol Learn Mem 90(2):347–357. https://doi.org/10.1016/j.nlm.2008.05.003 PubMedPubMedCentralCrossRef

Leussis MP, Bolivar VJ (2006) Habituation in rodents: a review of behavior, neurobiology, and genetics. Neurosci Biobehav Rev 30(7):1045–1064. https://doi.org/10.1016/j.neubiorev.2006.03.006 PubMedCrossRef

Levita L, Hoskin R, Champi S (2012) Avoidance of harm and anxiety: a role for the nucleus accumbens. Neuroimage 62(1):189–198. https://doi.org/10.1016/j.neuroimage.2012.04.059 PubMedCrossRef

Levy J (1977) The mammalian brain and the adaptive advantage of cerebral asymmetry. Ann N Y Acad Sci 299:264–272PubMedCrossRef

Luskin MB, Price JL (1983) The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J Comp Neurol 216(3):264–291. https://doi.org/10.1002/cne.902160305 PubMedCrossRef

Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897–931. https://doi.org/10.1146/annurev.neuro.24.1.897 PubMedCrossRef

Maren S (2016) Parsing Reward and Aversion in the Amygdala. Neuron 90(2):209–211. https://doi.org/10.1016/j.neuron.2016.04.011 PubMedCrossRef

Maren S, Phan KL, Liberzon I (2013) The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 14(6):417–428. https://doi.org/10.1038/nrn3492 PubMedPubMedCentralCrossRef

McDiarmid TA, Bernardos AC, Rankin CH (2017) Habituation is altered in neuropsychiatric disorders-a comprehensive review with recommendations for experimental design and analysis. Neurosci Biobehav Rev. https://doi.org/10.1016/j.neubiorev.2017.05.028 PubMed

Meunier M, Bachevalier J, Mishkin M, Murray EA (1993) Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J Neurosci 13(12):5418–5432PubMed

Michaelides M, Anderson SAR, Ananth M, Smirnov D, Thanos PK, Neumaier JF, Wang G-J, Volkow ND, Hurd YL (2013) Whole-brain circuit dissection in free-moving animals reveals cell-specific mesocorticolimbic networks. J Clin Invest 123(12):5342–5350CrossRef

Motta SC, Carobrez AP, Canteras NS (2017) The periaqueductal gray and primal emotional processing critical to influence complex defensive responses, fear learning and reward seeking. Neurosci Biobehav Rev 76(Pt A):39–47. https://doi.org/10.1016/j.neubiorev.2016.10.012 PubMedCrossRef

Nakamura K (1999) Auditory spatial discriminatory and mnemonic neurons in rat posterior parietal cortex. J Neurophysiol 82(5):2503–2517PubMedCrossRef

Neirinckx RD, Canning LR, Piper IM, Nowotnik DP, Pickett RD, Holmes RA, Volkert WA, Forster AM, Weisner PS, Marriott JA et al (1987) Technetium-99m d,l-HM-PAO: a new radiopharmaceutical for SPECT imaging of regional cerebral blood perfusion. J Nucl Med 28(2):191–202PubMed

Ohl FW, Scheich H (2005) Learning-induced plasticity in animal and human auditory cortex. Curr Opin Neurobiol 15(4):470–477. https://doi.org/10.1016/j.conb.2005.07.002 PubMedCrossRef

Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th edn. Academic Press, Cambridge

Pezze MA, Feldon J (2004) Mesolimbic dopaminergic pathways in fear conditioning. Prog Neurobiol 74(5):301–320. https://doi.org/10.1016/j.pneurobio.2004.09.004 PubMedCrossRef

Phelps EA, O’Connor KJ, Gatenby JC, Gore JC, Grillon C, Davis M (2001) Activation of the left amygdala to a cognitive representation of fear. Nat Neurosci 4(4):437–441. https://doi.org/10.1038/86110 PubMedCrossRef

Pine DS, Grun J, Maguire EA, Burgess N, Zarahn E, Koda V, Fyer A, Szeszko PR, Bilder RM (2002) Neurodevelopmental aspects of spatial navigation: a virtual reality fMRI study. Neuroimage 15(2):396–406. https://doi.org/10.1006/nimg.2001.0988 PubMedCrossRef

Pitkanen A, Pikkarainen M, Nurminen N, Ylinen A (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann N Y Acad Sci 911:369–391PubMedCrossRef

Pothuizen HH, Davies M, Albasser MM, Aggleton JP, Vann SD (2009) Granular and dysgranular retrosplenial cortices provide qualitatively different contributions to spatial working memory: evidence from immediate-early gene imaging in rats. Eur J Neurosci 30(5):877–888. https://doi.org/10.1111/j.1460-9568.2009.06881.x PubMedCrossRef

Riedel A, Gruss M, Bock J, Braun K (2010) Impaired active avoidance learning in infant rats appears to be related to insufficient metabolic recruitment of the lateral septum. Neurobiol Learn Mem 93(2):275–282. https://doi.org/10.1016/j.nlm.2009.11.001 pii]PubMedCrossRef

Rizvi TA, Ennis M, Behbehani MM, Shipley MT (1991) Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J Comp Neurol 303(1):121–131. https://doi.org/10.1002/cne.903030111 PubMedCrossRef

Rogan MT, Staubli UV, Ledoux JE (1997) Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390(6660):604–607PubMedCrossRef

Savonenko AV, Danilets AV, Zielinski K (1998) [The study of individual differences as a method for dividing into stages the acquisition of a complex reflex]. Zh Vyssh Nerv Deiat Im I P Pavlova 48(2):240–250PubMed

Savonenko A, Werka T, Nikolaev E, Zielinski K, Kaczmarek L (2003) Complex effects of NMDA receptor antagonist APV in the basolateral amygdala on acquisition of two-way avoidance reaction and long-term fear memory. Learn Mem 10(4):293–303. https://doi.org/10.1101/lm.58803 PubMedPubMedCentralCrossRef

Scheich H, Brosch M (2013) Task-related activation of auditory cortex. In: Neural correlates of auditory cognition. Springer, New York, pp 45–81CrossRef

Scott JW, McBride RL, Schneider SP (1980) The organization of projections from the olfactory bulb to the piriform cortex and olfactory tubercle in the rat. J Comp Neurol 194(3):519–534. https://doi.org/10.1002/cne.901940304 PubMedCrossRef

Sheth SA, Mian MK, Patel SR, Asaad WF, Williams ZM, Dougherty DD, Bush G, Eskandar EN (2012) Human dorsal anterior cingulate cortex neurons mediate ongoing behavioural adaptation. Nature 488(7410):218–221. https://doi.org/10.1038/nature11239 PubMedPubMedCentralCrossRef

Stark H, Scheich H (1997) Dopaminergic and serotonergic neurotransmission systems are differentially involved in auditory cortex learning: a long-term microdialysis study of metabolites. J Neurochem 68(2):691–697PubMedCrossRef

Stark H, Bischof A, Wagner T, Scheich H (2001) Activation of the dopaminergic system of medial prefrontal cortex of gerbils during formation of relevant associations for the avoidance strategy in the shuttle-box. Prog Neuropsychopharmacol Biol Psychiatry 25(2):409–426PubMedCrossRef

Stark H, Rothe T, Wagner T, Scheich H (2004) Learning a new behavioral strategy in the shuttle-box increases prefrontal dopamine. Neuroscience 126(1):21–29PubMedCrossRef

Steffenach HA, Witter M, Moser MB, Moser EI (2005) Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45(2):301–313. https://doi.org/10.1016/j.neuron.2004.12.044 PubMedCrossRef

Strange BA, Fletcher PC, Henson RN, Friston KJ, Dolan RJ (1999) Segregating the functions of human hippocampus. Proc Natl Acad Sci U S A 96(7):4034–4039PubMedPubMedCentralCrossRef

Strange BA, Witter MP, Lein ES, Moser EI (2014) Functional organization of the hippocampal longitudinal axis. Nat Rev Neurosci 15(10):655–669. https://doi.org/10.1038/nrn3785 PubMedCrossRef

Sullivan RM, Gratton A (1999) Lateralized effects of medial prefrontal cortex lesions on neuroendocrine and autonomic stress responses in rats. J Neurosci 19(7):2834–2840PubMed

Sullivan RM, Gratton A (2002) Behavioral effects of excitotoxic lesions of ventral medial prefrontal cortex in the rat are hemisphere-dependent. Brain Res 927(1):69–79PubMedCrossRef

Suzuki WA, Naya Y (2014) The perirhinal cortex. Annu Rev Neurosci 37:39–53. https://doi.org/10.1146/annurev-neuro-071013-014207 PubMedCrossRef

Tervaniemi M, Hugdahl K (2003) Lateralization of auditory-cortex functions. Brain Res Brain Res Rev 43(3):231–246PubMedCrossRef

Thanos PK, Robison L, Nestler EJ, Kim R, Michaelides M, Lobo M-K, Volkow ND (2013) Mapping brain metabolic connectivity in awake rats with μPET and optogenetic stimulation. J Neurosci 33(15):6343–6349 PubMedPubMedCentralCrossRef

Thiel CM, Huston JP, Schwarting RK (1998) Hippocampal acetylcholine and habituation learning. Neuroscience 85(4):1253–1262PubMedCrossRef

Thiel CM, Muller CP, Huston JP, Schwarting RK (1999) High versus low reactivity to a novel environment: behavioural, pharmacological and neurochemical assessments. Neuroscience 93(1):243–251PubMedCrossRef

Torrealba F, Valdes JL (2008) The parietal association cortex of the rat. Biol Res 41(4):369–377PubMedCrossRef

Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28(4):575–589. https://doi.org/10.1017/S0140525X05000105 discussion 589–633.PubMed

van Veen V, Cohen JD, Botvinick MM, Stenger VA, Carter CS (2001) Anterior cingulate cortex, conflict monitoring, and levels of processing. Neuroimage 14(6):1302–1308. https://doi.org/10.1006/nimg.2001.0923 PubMedCrossRef

VanElzakker 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(12):899–908. https://doi.org/10.1101/lm.1196508 PubMedPubMedCentralCrossRef

Vankov A, Herve-Minvielle A, Sara SJ (1995) Response to novelty and its rapid habituation in locus coeruleus neurons of the freely exploring rat. Eur J Neurosci 7(6):1180–1187PubMedCrossRef

Vianna MR, Alonso M, Viola H, Quevedo J, de Paris F, Furman M, de Stein ML, Medina JH, Izquierdo I (2000) Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat. Learn Mem 7(5):333–340PubMedPubMedCentralCrossRef

Vincenz D, Wernecke KEA, Fendt M, Goldschmidt J (2017) Habenula and interpeduncular nucleus differentially modulate predator odor-induced innate fear behavior in rats. Behav Brain Res 332:164–171. https://doi.org/10.1016/j.bbr.2017.05.053 PubMedCrossRef

Weinberger NM (2004) Specific long-term memory traces in primary auditory cortex. Nat Rev Neurosci 5(4):279–290. https://doi.org/10.1038/nrn1366 PubMedPubMedCentralCrossRef

Weinberger NM, Diamond DM (1987) Physiological plasticity in auditory cortex: rapid induction by learning. Prog Neurobiol 29(1):1–55PubMedCrossRef

Wesson DW, Wilson DA (2011) Sniffing out the contributions of the olfactory tubercle to the sense of smell: hedonics, sensory integration, and more? Neurosci Biobehav Rev 35(3):655–668. https://doi.org/10.1016/j.neubiorev.2010.08.004 PubMedCrossRef

Wetzel W, Ohl FW, Wagner T, Scheich H (1998) Right auditory cortex lesion in Mongolian gerbils impairs discrimination of rising and falling frequency-modulated tones. Neurosci Lett 252(2):115–118PubMedCrossRef

Wirtshafter D (2005) Cholinergic involvement in the cortical and hippocampal Fos expression induced in the rat by placement in a novel environment. Brain Res 1051(1–2):57–65. https://doi.org/10.1016/j.brainres.2005.05.052 PubMedCrossRef

Wyss JM, Van Groen T (1992) Connections between the retrosplenial cortex and the hippocampal formation in the rat: a review. Hippocampus 2(1):1–11. https://doi.org/10.1002/hipo.450020102 PubMedCrossRef

Yoder RM, Clark BJ, Taube JS (2011) Origins of landmark encoding in the brain. Trends Neurosci 34(11):561–571. https://doi.org/10.1016/j.tins.2011.08.004 PubMedPubMedCentralCrossRef

Zhu XO, McCabe BJ, Aggleton JP, Brown MW (1997) Differential activation of the rat hippocampus and perirhinal cortex by novel visual stimuli and a novel environment. Neurosci Lett 229(2):141–143PubMedCrossRef

Title: Comparing brain activity patterns during spontaneous exploratory and cue-instructed learning using single photon-emission computed tomography (SPECT) imaging of regional cerebral blood flow in freely behaving rats
Authors: A. Mannewitz
J. Bock
S. Kreitz
A. Hess
J. Goldschmidt
H. Scheich
Katharina Braun
Publication date: 01-05-2018
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 4/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-017-1605-x

At a glance: The STEP trials

Springer Medicine

Comparing brain activity patterns during spontaneous exploratory and cue-instructed learning using single photon-emission computed tomography (SPECT) imaging of regional cerebral blood flow in freely behaving rats

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2018

The lateralized arcuate fasciculus in developmental pitch disorders among mandarin amusics: left for speech and right for music

Organization of auditory areas in the superior temporal gyrus of marmoset monkeys revealed by real-time optical imaging

Cortical and subcortical connections of parietal and premotor nodes of the monkey hand mirror neuron network

Repeated shock stress facilitates basolateral amygdala synaptic plasticity through decreased cAMP-specific phosphodiesterase type IV (PDE4) expression

Disentangling brain activity related to the processing of emotional visual information and emotional arousal

Translaminar circuits formed by the pyramidal cells in the superficial layers of cat visual cortex