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Plasticity in the Interoceptive System

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The Plastic Brain

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1015))

Abstract

The most outstanding manifestations of the plastic capacities of brain circuits and their neuronal and synaptic components in the adult CNS are learning and memory. A reduced number of basic plastic mechanisms underlie learning capacities at many levels and regions of the brain. The interoceptive system is no exception, and some of the most studied behavioral changes that involve learning and memory engage the interoceptive pathways at many levels of their anatomical and functional organization.

In this chapter, we will review four examples of learning, mostly in rats, where the interoceptive system has a role. In the case of conditioned taste aversion, the interoceptive system is of outstanding importance. In drug addiction, the role of the insular cortex – the highest level of the interoceptive system– is unusual and complex, as many forebrain regions are engaged by the process of addiction. In the third example, neophobia, the gustatory region of the insular cortex plays a major role. Finally, the role of different areas of the insular cortex in different processes of aversive memory, particularly fear conditioning, will be reviewed.

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Abbreviations

BLA:

Basolateral amygdala

CTA:

Conditioned taste aversion

ERK:

Extracellular signal-regulated kinases

IC:

Insular cortex

MAPK:

Mitogen-activated protein kinases

NMDA:

N-Methyl-D-aspartate

NTS:

Nucleus of the solitary tract

pIC:

Posterior insular cortex

RAIC:

Rostral agranular insular cortex

TRN:

Thalamic reticular nucleus

VPLpc:

Ventroposterolateral parvicellular thalamic nucleus

VPMpc:

Ventroposteromedial parvicellular thalamic nucleus

References

  • Aberman JE, Ward SJ, Salamone JD (1998) Effects of dopamine antagonists and accumbens dopamine depletions on time-constrained progressive-ratio performance. Pharmacol Biochem Behav 61:341–348

    Article  CAS  PubMed  Google Scholar 

  • Acuña-Goycolea C, Fuentealba P, Torrealba F (2000) Anatomical substrate for separate processing of ascending and descending visceral information in the nucleus of the solitary tract of the rat. Brain Res 883:229–232

    Article  PubMed  Google Scholar 

  • Allen G, Saper CB, Hurley KM, Cechetto DF (1991) Organization of visceral and limbic connections in the insular cortex of the rat. J Comp Neurol 311(1):1–16

    Article  CAS  PubMed  Google Scholar 

  • Alves FH, Gomes FV, Reis DG, Crestani CC, Correa FM, Guimaraes FS, Resstel LB (2013) Involvement of the insular cortex in the consolidation and expression of contextual fear conditioning. Eur J Neurosci 38:2300–2307

    Article  PubMed  Google Scholar 

  • Andrew D, Craig AD (2001) Spinothalamic lamina I neurons selectively sensitive to histamine: a central neural pathway for itch. Nat Neurosci 4:72–77

    Article  CAS  PubMed  Google Scholar 

  • Berman DE, Hazvi S, Rosenblum K, Seger R, Dudai Y (1998) Specific and differential activation of mitogen-activated protein kinase cascades by unfamiliar taste in the insular cortex of the behaving rat. J Neurosci 18:10037–10044

    CAS  PubMed  Google Scholar 

  • Bermúdez-Rattoni F, McGaugh JL (1991) Insular cortex and amygdala lesions differentially affect acquisition on inhibitory avoidance and conditioned taste aversion. Brain Res 549:165–170

    Article  PubMed  Google Scholar 

  • Bermúdez-Rattoni F, Introini-Collison I, Coleman-Mesches K, McGaugh JL (1997) Insular cortex and amygdala lesions induced after aversive training impair retention: effects of degree of training. Neurobiol Learn Mem 67:57–63

    Article  PubMed  Google Scholar 

  • Bermúdez-Rattoni F, Ramírez-Lugo L, Gutiérrez R, Miranda MI (2004) Molecular signals into the insular cortex and amygdala during aversive gustatory memory formation. Cell Mol Neurobiol 24:25–36

    Article  PubMed  Google Scholar 

  • Blessing WW (1997) The lower brainstem and bodily homeostasis. Oxford University Press, Oxford

    Google Scholar 

  • Bozon B, Davis S, Laroche S (2003) A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40:695–701

    Article  CAS  PubMed  Google Scholar 

  • Campeau S, Davis M (1995) Involvement of subcortical and cortical afferent to the lateral nucleus of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci 15(3):2312–2327

    CAS  PubMed  Google Scholar 

  • Casanova JP, Madrid C, Contreras M, Rodríguez M, Vasquez M, Torrealba F (2016) A role for the interoceptive insular cortex in the consolidation of learned fear. Behav Brain Res 296:70–77

    Article  PubMed  Google Scholar 

  • Cechetto DF, Saper CB (1987) Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat. J Comp Neurol 262:27–45

    Article  CAS  PubMed  Google Scholar 

  • Cechetto DF, Saper CB (1990) Role of the cerebral cortex in autonomic function. In: Loewy AD, Spyer KM (eds) Central regulation of autonomic functions. Oxford University Press, Oxford, pp 208–223

    Google Scholar 

  • Christianson JP, Benison AM, Jennings J, Sandsmark EK, Amat J, Kaufman RD, Baratta MV, Paul ED, Campeau S, Watkins LR, Barth DS, Maier SF (2008) The sensory insular cortex mediates the stress-buffering effects of safety signals but not behavioral control. J Neurosci 28:13703–13711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christianson JP, Jennings JH, Ragole T, Flyer JG, Benison AM, Barth DS, Watkins LR, Maier SF (2011) Safety signals mitigate the consequences of uncontrollable stress via a circuit involving the sensory insular cortex and bed nucleus of the stria terminalis. Biol Psychiatry 70:458–464

    Article  PubMed  PubMed Central  Google Scholar 

  • Claps A, Torrealba F (1988) The carotid body connections: a WGA-HRP study in the cat. Brain Res 455(1):123–133

    Article  CAS  PubMed  Google Scholar 

  • Condé F, Audinat E, Maire-Lepoivre E, Crépel F (1995) Afferent connections of the medial frontal cortex of the rat. A study using retrograde transport of fluorescent dyes. I. Thalamic afferents. Brain Res Bull 24:341–354

    Article  Google Scholar 

  • Contreras M, Ceric F, Torrealba F (2007) Inactivation of the interoceptive insula disrupts drug craving and malaise induced by lithium. Science 318:655–658

    Article  CAS  PubMed  Google Scholar 

  • Contreras M, Billeke P, Vicencio S, Madrid C, Perdomo G, Gonzalez M, Torrealba F (2012) A role for the insular cortex in long-term memory for context-evoked drug craving in rats. Neuropsychopharmacology 37:2101–2108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666

    Article  CAS  PubMed  Google Scholar 

  • Craig AD (2004) Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13:500–505

    Article  Google Scholar 

  • Dunn LT, Everitt BJ (1988) Double dissociations of the effects of amygdala and insular cortex lesions on conditioned taste aversion, passive avoidance, and neophobia in the rat using the excitotoxin ibotenic acid. Behav Neurosci 102:3–23

    Article  CAS  PubMed  Google Scholar 

  • Erb S, Hitchcott PK, Rajabi H, Mueller D, Shaham Y, Stewart J (2000) Alpha-2 adrenergic receptor agonists block stress-induced reinstatement of cocaine seeking. Neuropsychopharmacology 23(2):138–150

    Article  CAS  PubMed  Google Scholar 

  • Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481–1489

    Article  CAS  PubMed  Google Scholar 

  • Everitt BJ, Robbins TW (2013) From the ventral to the dorsal striatum: devolving views of their roles in drug addiction. Neurosci Biobehav Rev 79:1946–1954

    Article  Google Scholar 

  • Everitt BJ, Wolf ME (2002) Psychomotor stimulant addiction: a neural systems perspective. J Neurosci 22:3312–3320

    CAS  PubMed  Google Scholar 

  • Figueroa-Guzmán Y, Reilly S (2008) NMDA receptors in the basolateral amygdala and gustatory neophobia. Brain Res 1210:200–203

    Article  PubMed  PubMed Central  Google Scholar 

  • Figueroa-Guzmán Y, Kuo JS, Reilly S (2006) NMDA receptor antagonist MK-801 infused into the insular cortex prevents the attenuation of gustatory neophobia in rats. Brain Res 1114:183–186

    Article  PubMed  Google Scholar 

  • Gabbott PL, Warner TA, Jays PR, Bacon SJ (2003) Areal and synaptic interconnectivity of prelimbic (area 32), infralimbic (area 25) and insular cortices in the rat. Brain Res 993:59–71

    Article  CAS  PubMed  Google Scholar 

  • Garcia J, Hankins WG, Rusiniak KW (1974) Behavioral regulation of the milieu interne in man and rat. Science 185:824–831

    Article  CAS  PubMed  Google Scholar 

  • Gauriau C, Bernard JF (2002) Pain pathways and parabrachial circuits in the rat. Exp Physiol 87:251–258

    Article  PubMed  Google Scholar 

  • Gauriau C, Bernard JF (2004) A comparative reappraisal of projections from the superficial laminae of the dorsal horn in the rat: the forebrain. J Comp Neurol 468:24–56

    Article  PubMed  Google Scholar 

  • Guldin W, Markowitsch HJ (1983) Cortical and thalamic afferent connections of the insular and adjacent cortex of the rat. J Comp Neurol 215(2):135–153

    Article  CAS  PubMed  Google Scholar 

  • Gutiérrez R, Téllez LA, Bermúdez-Rattoni F (2003) Blockade of cortical muscarinic but not NMDA receptors prevents a novel taste from becoming familiar. Eur J Neurosci 17:1556–1562

    Article  PubMed  Google Scholar 

  • Hall J, Thomas KL, Everitt BJ (2001) Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: selective activation of hippocampal CA1 neurons during the recall of contextual memories. J Neurosci 21:2186–2193

    CAS  PubMed  Google Scholar 

  • Hoover WB, Vertes RP (2007) Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 212:149–179

    Article  PubMed  Google Scholar 

  • Iggo A (1986) Afferent C-fibres and visceral sensation. In: Cervero F, Morrison JFB (eds) Visceral sensation. Elsevier, Amsterdam, pp 29–36

    Chapter  Google Scholar 

  • Jasmin L, Burkey AR, Granato A, Ohara PT (2004) Rostral agranular insular cortex and pain areas of the central nervous system: a tract-tracing study in the rat. J Comp Neurol 468:425–440

    Article  PubMed  Google Scholar 

  • Kalia M, Richter D (1988) Rapidly adapting pulmonary receptor afferents: II. Fine structure and synaptic organization of central terminal processes in the nucleus of the tractus solitarius. J Comp Neurol 274:574–594

    Article  CAS  PubMed  Google Scholar 

  • Kiefer SW, Rusiniak KW, Garcia J (1982) Flavor-illness aversions: gustatory neocortex ablations disrupt taste but not taste-potentiated odor cues. J Comp Physiol Psychol 96:540–548

    Article  CAS  PubMed  Google Scholar 

  • Koob GF, Le Moal M (2005) Plasticity of reward neurocircuitry and the ‘dark side’ of drug addiction. Nat Neurosci 8:1442–1444

    Article  CAS  PubMed  Google Scholar 

  • Koob GF, Le Moal M (2006) Neurobiology of addiction. Academic, London

    Google Scholar 

  • Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238

    Article  PubMed  Google Scholar 

  • Krettek JE, Price JL (1977) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171(2):157–191

    Article  CAS  PubMed  Google Scholar 

  • Lacroix L, Spinelli S, Heidbreder CA, Feldon J (2000) Differential role of the medial and lateral prefrontal cortices in fear and anxiety. Behav Neurosci 114:1119–1130

    Article  CAS  PubMed  Google Scholar 

  • LeDoux JE (1996) The emotional brain. Simon and Schuster, New York

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lee JL, Everitt BJ, Thomas KL (2004) Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science 304:839–843

    Article  CAS  PubMed  Google Scholar 

  • Lee JL, Di Ciano P, Thomas KL, Everitt BJ (2005) Disrupting reconsolidation of drug memories reduces cocaine seeking behavior. Neuron 47:795–801

    Article  CAS  PubMed  Google Scholar 

  • Lee JL, Milton AL, Everitt BJ (2006) Cue-induced cocaine seeking and relapse are reduced by disruption of drug memory reconsolidation. J Neurosci 26:5881–5887

    Article  CAS  PubMed  Google Scholar 

  • Li CL, Zhu N, Meng XL, Li YH, Sui N (2013) Effects of inactivating the agranular or granular insular cortex on the acquisition of the morphine-induced conditioned place preference and naloxone-precipitated conditioned place aversion in rats. J Psychopharmacol 27(9):837–844

    Article  PubMed  Google Scholar 

  • Lin JY, Reilly S (2012) Amygdala-gustatory insular cortex connections and taste neophobia. Behav Brain Res 235:182–188

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin JY, Roman C, Arthurs J, Reilly S (2012) Taste neophobia and c-Fos expression in the rat brain. Brain Res 1448:82–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin JY, Arthurs J, Reilly S (2015) Gustatory insular cortex, aversive taste memory and taste neophobia. Neurobiol Learn Mem 119:77–84

    Article  PubMed  PubMed Central  Google Scholar 

  • London ED, Ernst M, Grant S, Bonson K, Weinstein A (2000) Orbitofrontal cortex and human drug abuse: functional imaging. Cereb Cortex 10:334–342

    Article  CAS  PubMed  Google Scholar 

  • Mcdonald AJ, Mascagni F, Guo L (1996) Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 71:55–75

    Article  CAS  PubMed  Google Scholar 

  • Mesulam M, Mufson EJ (1982) Insula of the old world monkey I. Architectonics in the insulo-orbito-temporal component of the paralimbic brain. J Comp Neuro 212:1–22

    Article  CAS  Google Scholar 

  • Morgan MA, LeDoux JE (1999) Contribution of ventrolateral prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Neurobiol Learn Mem 72(3):244–251

    Article  CAS  PubMed  Google Scholar 

  • Nerad L, Ramirez-Amaya V, Ormsby CE, Bermudez-Rattoni F (1996) Differential effects of anterior and posterior insular cortex lesions on the acquisition of conditioned taste aversion and spatial learning. Neurobiol Learn Mem 66:44–50

    Article  CAS  PubMed  Google Scholar 

  • O’Brien CP, Childress AR, Ehrman R, Robbins SJ (1998) Conditioning factors in drug abuse: can they explain compulsion? J Psychopharmacol 12:15–22

    Article  PubMed  Google Scholar 

  • Öngur D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats; monkeys and humans. Cerb Cortex 10(3):206–219

    Article  Google Scholar 

  • Pushparaj A, Le Foll B (2015) Involvement of the caudal granular insular cortex in alcohol self-administration in rats. Behav Brain Res 293:203–207

    Article  CAS  PubMed  Google Scholar 

  • Ray J, Price JL (1992) The organization of the thalamocortical connections of the mediodorsal thalamic nucleus in the rat, related to the ventral forebrain-prefrontal cortex topography. J Comp Neurol 323(2):167–197

    Article  CAS  PubMed  Google Scholar 

  • Reilly S, Bornovalova MA (2005) Conditioned taste aversion and amygdala lesions in the rat: a critical review. Neurosci Biobehav Rev 29:1067–1088

    Article  PubMed  Google Scholar 

  • Reynolds SM, Zahm DS (2005) Specificity in the projections of prefrontal and insular cortex to ventral striatopallidum and the extended amygdala. J Neurosci 25:11757–11767

    Article  CAS  PubMed  Google Scholar 

  • Romanski L, LeDoux JE (1992) Bilateral destruction of neocortical and perirhinal projection targets of the acoustic thalamus does not disrupt auditory fear conditioning. Neurosci Lett 142(2):228–232

    Article  CAS  PubMed  Google Scholar 

  • Rosen J, Hitchcock JM, Miserendino MJ, Falls WA, Campeau S, Davis M (1992) Lesions of the perirhinal cortex but not of the frontal, medial prefrontal, visual, or insular cortex block fear-potentiated startle using a visual conditioned stimulus. J Neurosci 12(12):4624–4633

    CAS  PubMed  Google Scholar 

  • Rosenblum K, Meiri N, Dudai Y (1993) Taste memory: the role of protein synthesis in gustatory cortex. Behav Neural Biol 59:49–56

    Article  CAS  PubMed  Google Scholar 

  • Rosenblum K, Berman DE, Hazvi S, Lamprecht R, Dudai Y (1997) NMDA receptor and the tyrosine phosphorylation of its 2B subunit in taste learning in the rat insular cortex. J Neurosci 17:5129–5135

    CAS  PubMed  Google Scholar 

  • Santini E, Ge H, Ren K, Peña de Ortiz S, Quirk GJ (2004) Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex. J Neurosci 24:5704–5710

    Article  CAS  PubMed  Google Scholar 

  • Saper CB (1982) Convergence of autonomic and limbic in the insular cortex of the rat. J Comp Neurol 210(2):163–173

    Article  CAS  PubMed  Google Scholar 

  • Saper CB (1995) The rat nervous system, 2nd edn. Academic, San Diego

    Google Scholar 

  • Schafe GE, Bernstein IL (1998) Forebrain contribution to the induction of a brainstem correlate of conditioned taste aversion. II. Insular (gustatory) cortex. Brain Res 800:40–47

    Article  CAS  PubMed  Google Scholar 

  • See RE (2002) Neural substrates of conditioned-cued relapse to drug-seeking behavior. Pharmacol Biochem Behav 71:517–529

    Article  CAS  PubMed  Google Scholar 

  • 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(2):213–242

    Article  CAS  PubMed  Google Scholar 

  • Shi CJ, Cassell MD (1998a) Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. J Comp Neurol 399:440–468

    Article  CAS  PubMed  Google Scholar 

  • Shi CJ, Cassell MD (1998b) Cascade projections from somatosensory cortex to the rat basolateral amygdala via the parietal insular cortex. J Comp Neurol 399:469–491

    Article  CAS  PubMed  Google Scholar 

  • Stehberg J, Acuña-Goycolea C, Ceric F, Torrealba F (2001) The visceral sector of the thalamic reticular nucleus in the rat. Neuroscience 106:745–755

    Article  CAS  PubMed  Google Scholar 

  • Torrealba F, Claps A (1988) The carotid sinus connections: a WGA- HRP study in the cat. Brain Res 455:134–143

    Article  CAS  PubMed  Google Scholar 

  • Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51(1):32–58

    Article  CAS  PubMed  Google Scholar 

  • Weiss F, Ciccocioppo R, Parsons LH, Katner S, Liu X, Zorrilla EP, Valdez GR, Ben-Shahar O, Angeletti S, Richter RR (2001) Compulsive drug-seeking behavior and relapse. Neuroadaptation, stress, and conditioning factors. Ann N Y Acad Sci 937:1–26

    Article  CAS  PubMed  Google Scholar 

  • Widdicombe JG (1998) Afferent receptors in the airways and cough. Respir Physiol 114(1):5–15

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Fernando Torrealba .

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Torrealba, F., Madrid, C., Contreras, M., Gómez, K. (2017). Plasticity in the Interoceptive System. In: von Bernhardi, R., Eugenín, J., Muller, K. (eds) The Plastic Brain. Advances in Experimental Medicine and Biology, vol 1015. Springer, Cham. https://doi.org/10.1007/978-3-319-62817-2_4

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