Beyond the hippocampus: The role of parahippocampal-prefrontal communication in context-modulated behavior

Aggleton, J. P., & Nelson, A. J. D. (2020). Distributed interactive brain circuits for object-in-place memory: A place for time? Brain Neurosci Adv, 4, 2398212820933471. https://doi.org/10.1177/2398212820933471. Agster, 2009, Cortical efferents of the perirhinal, postrhinal, and entorhinal cortices of the rat, Hippocampus, 19, 1159, 10.1002/hipo.20578 Agster, 2016, Subcortical connections of the perirhinal, postrhinal, and entorhinal cortices of the rat. II. efferents, Hippocampus, 26, 1213, 10.1002/hipo.22600 Albasser, 2009, Magnitude of the object recognition deficit associated with perirhinal cortex damage in rats: Effects of varying the lesion extent and the duration of the sample period, Behavioral Neuroscience, 123, 115, 10.1037/a0013829 Allen, 2020, The hippocampus, prefrontal cortex, and perirhinal cortex are critical to incidental order memory, Behavioural Brain Research, 379, 112215, 10.1016/j.bbr.2019.112215 Banerjee, 2020, Value-guided remapping of sensory cortex by lateral orbitofrontal cortex, Nature, 585, 245, 10.1038/s41586-020-2704-z Bardo, 2000, Conditioned place preference: What does it add to our preclinical understanding of drug reward?, Psychopharmacology (Berl), 153, 31, 10.1007/s002130000569 Barker, 2007, Recognition memory for objects, place, and temporal order: A disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex, Journal of Neuroscience, 27, 2948, 10.1523/JNEUROSCI.5289-06.2007 Barker, 2009, Critical role of the cholinergic system for object-in-place associative recognition memory, Learning & Memory, 16, 8, 10.1101/lm.1121309 Barker, 2011, When is the hippocampus involved in recognition memory?, Journal of Neuroscience, 31, 10721, 10.1523/JNEUROSCI.6413-10.2011 Barreiros, 2021, Organization of afferents along the anterior–posterior and medial–lateral axes of the rat orbitofrontal cortex, Neuroscience, 460, 53, 10.1016/j.neuroscience.2021.02.017 Barthas, 2017, Secondary motor cortex: Where ‘sensory’meets ‘motor’in the rodent frontal cortex, Trends in Neurosciences, 40, 181, 10.1016/j.tins.2016.11.006 Bianchi, 2018, Functional inactivation of the orbitofrontal cortex disrupts context-induced reinstatement of alcohol seeking in rats, Drug and Alcohol Dependence, 186, 102, 10.1016/j.drugalcdep.2017.12.045 Bouton, 2004, Context and behavioral processes in extinction, Learning & Memory, 11, 485, 10.1101/lm.78804 Bouton, 1979, Contextual control of the extinction of conditioned fear, Learning and Motivation, 10, 445, 10.1016/0023-9690(79)90057-2 Bradfield, 2020, Rodent medial and lateral orbitofrontal cortices represent unique components of cognitive maps of task space, Neuroscience & Biobehavioral Reviews, 108, 287, 10.1016/j.neubiorev.2019.11.009 Bucci, 2004, Deficits in attentional orienting following damage to the perirhinal or postrhinal cortices [article], Behavioral neuroscience, 118, 1117, 10.1037/0735-7044.118.5.1117 Bucci, 2000, Contributions of postrhinal and perirhinal cortex to contextual information processing, Behavioral neuroscience, 114, 882, 10.1037/0735-7044.114.5.882 Bucci, 2002, Contextual fear discrimination is impaired by damage to the postrhinal or perirhinal cortex, Behavioral Neuroscience, 116, 479, 10.1037/0735-7044.116.3.479 Burgess, 2016, Hunger-dependent enhancement of food cue responses in mouse postrhinal cortex and lateral amygdala, Neuron, 91, 1154, 10.1016/j.neuron.2016.07.032 Burwell, R., & Agster, K. (2008). Anatomy of the hippocampus and the declarative memory system. https://doi.org/10.1016/B978-012370509-9.00117-0. Burwell, 2001, Borders and cytoarchitecture of the perirhinal and postrhinal cortices in the rat, Journal of Comparative Neurology, 437, 17, 10.1002/cne.1267 Burwell, 1998, Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat, Journal of Comparative Neurology, 398, 179, 10.1002/(SICI)1096-9861(19980824)398:2<179::AID-CNE3>3.0.CO;2-Y Burwell, 1998, Perirhinal and postrhinal cortices of the rat: Interconnectivity and connections with the entorhinal cortex, Journal of Comparative Neurology, 391, 293, 10.1002/(SICI)1096-9861(19980216)391:3<293::AID-CNE2>3.0.CO;2-X Burwell, 2004, Perirhinal and postrhinal contributions to remote memory for context, In, 24, 11023 Burwell, 2003, Positional firing properties of postrhinal cortex neurons, Neuroscience, 119, 577, 10.1016/S0306-4522(03)00160-X Burwell, 2002, Basic anatomy of the parahippocampal region in monkeys and rats [Chapter], Oxford University Press Burwell, 1995, Perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain, Hippocampus, 5, 390, 10.1002/hipo.450050503 Bussey, 2002, Perirhinal cortex resolves feature ambiguity in complex visual discriminations, European Journal of Neuroscience, 15, 365, 10.1046/j.0953-816x.2001.01851.x Bussey, 2005, The perceptual-mnemonic/feature conjunction model of perirhinal cortex function, The Quarterly Journal of Experimental Psychology Section B, 58, 269, 10.1080/02724990544000004 Chakraborty, 2016, Variants of contextual fear conditioning induce differential patterns of Egr-1 activity within the young adult prefrontal cortex, Behavioural Brain Research, 302, 122, 10.1016/j.bbr.2016.01.018 Corcoran, 2007, Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears, Journal of Neuroscience, 27, 840, 10.1523/JNEUROSCI.5327-06.2007 Corodimas, 1995, Disruptive effects of posttraining perirhinal cortex lesions on conditioned fear: Contributions of contextual cues, Behavioral Neuroscience, 109, 613, 10.1037/0735-7044.109.4.613 Cross, 2013, The medial dorsal thalamic nucleus and the medial prefrontal cortex of the rat function together to support associative recognition and recency but not item recognition, Learning & Memory, 20, 41, 10.1101/lm.028266.112 Dalley, 2004, Prefrontal executive and cognitive functions in rodents: Neural and neurochemical substrates, Neuroscience & Biobehavioral Reviews, 28, 771, 10.1016/j.neubiorev.2004.09.006 Delatour, 2002, Projections from the parahippocampal region to the prefrontal cortex in the rat: Evidence of multiple pathways, European Journal of Neuroscience, 15, 1400, 10.1046/j.1460-9568.2002.01973.x Diana, 2007, Imaging recollection and familiarity in the medial temporal lobe: A three-component model, Trends in Cognitive Sciences, 11, 379, 10.1016/j.tics.2007.08.001 Eddy, 2016, Medial prefrontal cortex involvement in the expression of extinction and ABA renewal of instrumental behavior for a food reinforcer, Neurobiology of learning and memory, 128, 33, 10.1016/j.nlm.2015.12.003 Eichenbaum, 2017, Prefrontal-hippocampal interactions in episodic memory, Nature Reviews Neuroscience, 18, 547, 10.1038/nrn.2017.74 Eichenbaum, 2012, Towards a functional organization of episodic memory in the medial temporal lobe, Neuroscience & Biobehavioral Reviews, 36, 1597, 10.1016/j.neubiorev.2011.07.006 Eichenbaum, 2007, The medial temporal lobe and recognition memory, Annual Review of Neuroscience, 30, 123, 10.1146/annurev.neuro.30.051606.094328 Ennaceur, 1997, Spontaneous object recognition and object location memory in rats: The effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix, Experimental Brain Research, 113, 509, 10.1007/PL00005603 Estela, 2020 Estela-Pro, 2021, The anatomy and function of the postrhinal cortex, Behavioral Neuroscience Farovik, 2015, Orbitofrontal cortex encodes memories within value-based schemas and represents contexts that guide memory retrieval, Journal of Neuroscience, 35, 8333, 10.1523/JNEUROSCI.0134-15.2015 Feierstein, 2006, Representation of spatial goals in rat orbitofrontal cortex, Neuron, 51, 495, 10.1016/j.neuron.2006.06.032 Fraser, 2019, Occasion Setting, In (Vol., 133, 145 Frost, 2021, Anterior thalamic inputs are required for subiculum spatial coding, with associated consequences for hippocampal spatial memory, Journal of Neuroscience, 41, 6511, 10.1523/JNEUROSCI.2868-20.2021 Furtak, 2012, Single neuron activity and theta modulation in postrhinal cortex during visual object discrimination, Neuron, 76, 976, 10.1016/j.neuron.2012.10.039 Gilmartin, 2010, Trace and contextual fear conditioning require neural activity and NMDA receptor-dependent transmission in the medial prefrontal cortex, Learning & Memory, 17, 289, 10.1101/lm.1597410 Gilmartin, 2013, NR2A-and NR2B-containing NMDA receptors in the prelimbic medial prefrontal cortex differentially mediate trace, delay, and contextual fear conditioning, Learning & Memory, 20, 290, 10.1101/lm.030510.113 Hallock, 2013, Dissociable roles of the dorsal striatum and dorsal hippocampus in conditional discrimination and spatial alternation T-maze tasks, Neurobiology of Learning and Memory, 100, 108, 10.1016/j.nlm.2012.12.009 Hallock, 2013, Dynamic coding of dorsal hippocampal neurons between tasks that differ in structure and memory demand, Hippocampus, 23, 169, 10.1002/hipo.22079 Hannesson, 2004, Medial prefrontal cortex is involved in spatial temporal order memory but not spatial recognition memory in tests relying on spontaneous exploration in rats, Behavioural Brain Research, 153, 273, 10.1016/j.bbr.2003.12.004 Heimer-McGinn, 2017, Disconnection of the perirhinal and postrhinal cortices impairs recognition of objects in context but not contextual fear conditioning, Journal of Neuroscience, 37, 4819, 10.1523/JNEUROSCI.0254-17.2017 Hernandez, 2017, Medial prefrontal-perirhinal cortical communication is necessary for flexible response selection, Neurobiology of Learning and Memory, 137, 36, 10.1016/j.nlm.2016.10.012 Ho, J. W., & Burwell, R. D. (2014). Perirhinal and postrhinal functional inputs to the hippocampus. In Space, time and memory in the hippocampal formation (pp. 55-81). Springer. https://doi.org/https://doi.org/10.1007/978-3-7091-1292-2_3. Hok, 2007, Goal-related activity in hippocampal place cells, Journal of Neuroscience, 27, 472, 10.1523/JNEUROSCI.2864-06.2007 Hoover, 2007, Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat, Brain Structure and Function, 212, 149, 10.1007/s00429-007-0150-4 Hwang, 2018, Prefrontal connections of the perirhinal and postrhinal cortices in the rat, Behavioural brain research, 354, 8, 10.1016/j.bbr.2017.07.032 Hyman, 2012, Contextual encoding by ensembles of medial prefrontal cortex neurons, Proceedings of the National Academy of Sciences, 109, 5086, 10.1073/pnas.1114415109 Iordanova, 2009, The role of the hippocampus in mnemonic integration and retrieval: Complementary evidence from lesion and inactivation studies, European Journal of Neuroscience., 30, 2177, 10.1111/j.1460-9568.2009.07010.x Jay, 1991, Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin, Journal of Comparative Neurology, 313, 574, 10.1002/cne.903130404 Ji, 2007, Hippocampal involvement in contextual modulation of fear extinction, Hippocampus, 17, 749, 10.1002/hipo.20331 Jo, 2010, Perirhinal cortex is necessary for acquiring, but not for retrieving object–place paired association, Learning & Memory, 17, 97, 10.1101/lm.1620410 Kent, 2012, Dual functions of perirhinal cortex in fear conditioning, Hippocampus, 22, 2068, 10.1002/hipo.22058 Kerr, 2007, Functional neuroanatomy of the parahippocampal region: The lateral and medial entorhinal areas, Hippocampus, 17, 697, 10.1002/hipo.20315 Kholodar-Smith, 2008, Fear conditioning to discontinuous auditory cues requires perirhinal cortical function, Behavioral neuroscience, 122, 1178, 10.1037/a0012902 Kim, 2013, The prelimbic cortex is critical for context-dependent fear expression, Frontiers in Behavioral Neuroscience, 7, 73, 10.3389/fnbeh.2013.00073 Komorowski, 2009, Robust conjunctive item-place coding by hippocampal neurons parallels learning what happens where, Journal of Neuroscience, 29, 9918, 10.1523/JNEUROSCI.1378-09.2009 Kondo, 2014, Topographic organization of orbitofrontal projections to the parahippocampal region in rats, Journal of Comparative Neurology, 522, 772, 10.1002/cne.23442 Kreher, 2019, The perirhinal cortex supports spatial intertemporal choice stability, Neurobiology of Learning and Memory, 162, 36, 10.1016/j.nlm.2019.05.002 Lasseter, 2009, Involvement of the lateral orbitofrontal cortex in drug context-induced reinstatement of cocaine-seeking behavior in rats, European Journal of Neuroscience, 30, 1370, 10.1111/j.1460-9568.2009.06906.x Lasseter, 2011, Interaction of the basolateral amygdala and orbitofrontal cortex is critical for drug context-induced reinstatement of cocaine-seeking behavior in rats, Neuropsychopharmacology, 36, 711, 10.1038/npp.2010.209 Lee, 2008, The roles of the medial prefrontal cortex and hippocampus in a spatial paired-association task, Learning & Memory, 15, 357, 10.1101/lm.902708 Lindquist, 2004, Perirhinal cortex supports delay fear conditioning to rat ultrasonic social signals, Journal of Neuroscience, 24, 3610, 10.1523/JNEUROSCI.4839-03.2004 Liu, 2020, Orbitofrontal control of visual cortex gain promotes visual associative learning, Nature Communications, 11, 2784, 10.1038/s41467-020-16609-7 Logue, 2014, The neural and genetic basis of executive function: Attention, cognitive flexibility, and response inhibition, Pharmacology Biochemistry and Behavior, 123, 45, 10.1016/j.pbb.2013.08.007 Maren, 1997, Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats, Behavioural brain research, 88, 261, 10.1016/S0166-4328(97)00088-0 McKenna, 2004, Afferent projections to nucleus reuniens of the thalamus, The Journal of Comparative Neurology, 480, 115, 10.1002/cne.20342 Murphy, 2018, Organization of afferents to the orbitofrontal cortex in the rat, The Journal of Comparative Neurology, 526, 1498, 10.1002/cne.24424 Navawongse, 2013, Distinct pathways for rule-based retrieval and spatial mapping of memory representations in hippocampal neurons, Journal of Neuroscience, 33, 1002, 10.1523/JNEUROSCI.3891-12.2013 Norman, 2004, Impaired object recognition with increasing levels of feature ambiguity in rats with perirhinal cortex lesions, Behavioural Brain Research, 148, 79, 10.1016/S0166-4328(03)00176-1 Norman, 2005, Dissociable effects of lesions to the perirhinal cortex and the postrhinal cortex on memory for context and objects in rats, Behavioral Neuroscience, 119, 557, 10.1037/0735-7044.119.2.557 Olson, 2020, Secondary motor cortex transforms spatial information into planned action during navigation, Current Biology, 30, 1845, 10.1016/j.cub.2020.03.016 Orsini, 2011, Hippocampal and prefrontal projections to the basal amygdala mediate contextual regulation of fear after extinction, Journal of Neuroscience, 31, 17269, 10.1523/JNEUROSCI.4095-11.2011 Place, 2016, Bidirectional prefrontal-hippocampal interactions support context-guided memory, Nature Neuroscience, 19, 992, 10.1038/nn.4327 Potter, 2020, Perirhinal cortex inactivation produces retrieval deficits in fear extinction to a discontinuous visual stimulus, Behavioral Neuroscience, 134, 144, 10.1037/bne0000351 Qi, 2019, The glutamatergic postrhinal cortex-ventrolateral orbitofrontal cortex pathway regulates spatial memory retrieval, Neuroscience Bulletin, 35, 447, 10.1007/s12264-018-0325-4 Ramesh, 2018, Intermingled ensembles in visual association cortex encode stimulus identity or predicted outcome, Neuron, 100, 900, 10.1016/j.neuron.2018.09.024 Reep, 1987, Efferent connections of the rostral portion of medial agranular cortex in rats, Brain research bulletin, 19, 203, 10.1016/0361-9230(87)90086-4 Reep, 1990, Topographic organization in the corticocortical connections of medial agranular cortex in rats, Journal of Comparative Neurology, 294, 262, 10.1002/cne.902940210 Reep, 1984, Afferent connections of medial precentral cortex in the rat, Neuroscience Letters, 44, 247, 10.1016/0304-3940(84)90030-2 Rescorla, 1972, 64 Robinson, 2012, Identification of functional circuitry between retrosplenial and postrhinal cortices during fear conditioning, Journal of Neuroscience, 32, 12076, 10.1523/JNEUROSCI.2814-12.2012 Santos, 2017, Involvement of the prelimbic cortex in contextual fear conditioning with temporal and spatial discontinuity, Neurobiology of Learning and Memory, 144, 1, 10.1016/j.nlm.2017.05.003 Scharfman, 2000 Sharpe, 2015, The prelimbic cortex uses contextual cues to modulate responding towards predictive stimuli during fear renewal, Neurobiology of Learning and Memory, 118, 20, 10.1016/j.nlm.2014.11.005 Sharpe, 2019, An integrated model of action selection: Distinct modes of cortical control of striatal decision making, Annual Review of Psychology, 70, 53, 10.1146/annurev-psych-010418-102824 Siniscalchi, 2019, Enhanced population coding for rewarded choices in the medial frontal cortex of the mouse, Cerebral Cortex, 29, 4090, 10.1093/cercor/bhy292 Sugden, 2020, Cortical reactivations of recent sensory experiences predict bidirectional network changes during learning, Nature Neuroscience, 23, 981, 10.1038/s41593-020-0651-5 Sul, 2011, Role of rodent secondary motor cortex in value-based action selection, Nature Neuroscience, 14, 1202, 10.1038/nn.2881 Suter, 2013, Perirhinal and postrhinal, but not lateral entorhinal, cortices are essential for acquisition of trace eyeblink conditioning, Learning & Memory, 20, 80, 10.1101/lm.028894.112 Suzuki, 2014, The perirhinal cortex, Annual Review of Neuroscience, 37, 39, 10.1146/annurev-neuro-071013-014207 Tam, 2015, Relative recency influences object-in-context memory, Behavioural Brain Research, 281, 250, 10.1016/j.bbr.2014.12.024 Tomás Pereira, 2016, Subcortical connections of the perirhinal, postrhinal, and entorhinal cortices of the rat, I. afferents. Hippocampus, 26, 1189, 10.1002/hipo.22603 Trask, 2017, Inactivation of the prelimbic cortex attenuates context-dependent operant responding, Journal of Neuroscience, 37, 2317, 10.1523/JNEUROSCI.3361-16.2017 Trask, 2017, Occasion setting, inhibition, and the contextual control of extinction in Pavlovian and instrumental (operant) learning, Behavioural Processes, 137, 64, 10.1016/j.beproc.2016.10.003 Urban, 2014, Transient inactivation of the medial prefrontal cortex impairs performance on a working memory-dependent conditional discrimination task, Behavioral Neuroscience, 128, 639, 10.1037/bne0000020 Vertes, 2006, Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat, The Journal of Comparative Neurology, 499, 768, 10.1002/cne.21135 Vertes, 2007, Nucleus reuniens of the midline thalamus: Link between the medial prefrontal cortex and the hippocampus, Brain Research Bulletin, 71, 601, 10.1016/j.brainresbull.2006.12.002 Vertes, 2015, Limbic circuitry of the midline thalamus, Neuroscience & Biobehavioral Reviews, 54, 89, 10.1016/j.neubiorev.2015.01.014 Wagner, 1972, Inhibition in Pavlovian conditioning: Application of a theory, Inhibition and Learning, 301 Wang, 2016, Renewal of extinguished fear activates ventral hippocampal neurons projecting to the prelimbic and infralimbic cortices in rats, Neurobiology of learning and memory, 134, 38, 10.1016/j.nlm.2016.04.002 Warburton, 2015, Neural circuitry for rat recognition memory, Behavioural Brain Research, 285, 131, 10.1016/j.bbr.2014.09.050 Wikenheiser, 2016, Over the river, through the woods: Cognitive maps in the hippocampus and orbitofrontal cortex, Nature Reviews Neuroscience, 17, 513, 10.1038/nrn.2016.56 Wilson, 2014, Orbitofrontal cortex as a cognitive map of task space, Neuron, 81, 267, 10.1016/j.neuron.2013.11.005 Winocur, 2013, Hippocampal lesions produce both nongraded and temporally graded retrograde amnesia in the same rat, Hippocampus, 23, 330, 10.1002/hipo.22093 Winters, 2005, Transient inactivation of perirhinal cortex disrupts encoding, retrieval, and consolidation of object recognition memory, Journal of Neuroscience, 25, 52, 10.1523/JNEUROSCI.3827-04.2005 Xiang, 1998, Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe, Neuropharmacology, 37, 657, 10.1016/S0028-3908(98)00030-6 Zelikowsky, 2013, Prefrontal microcircuit underlies contextual learning after hippocampal loss, Proceedings of the National Academy of Sciences, 110, 9938, 10.1073/pnas.1301691110 Zelikowsky, 2014, Neuronal ensembles in amygdala, hippocampus, and prefrontal cortex track differential components of contextual fear, Journal of Neuroscience, 34, 8462, 10.1523/JNEUROSCI.3624-13.2014