1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Neuroscience
  4. Volume 46, 2023
  5. Article

Annual Review of Neuroscience

Volume 46, 2023

Cognition from the Body-Brain Partnership: Exaptation of Memory

Abstract

Examination of cognition has historically been approached from language and introspection. However, human language–dependent definitions ignore the evolutionary roots of brain mechanisms and constrain their study in experimental animals. We promote an alternative view, namely that cognition, including memory, can be explained by exaptation and expansion of the circuits and algorithms serving bodily functions. Regulation and protection of metabolic and energetic processes require time-evolving brain computations enabling the organism to prepare for altered future states. Exaptation of such circuits was likely exploited for exploration of the organism's niche. We illustrate that exploration gives rise to a cognitive map, and in turn, environment-disengaged computation allows for mental travel into the past (memory) and the future (planning). Such brain-body interactions not only occur during waking but also persist during sleep. These exaptation steps are illustrated by the dual, endocrine-homeostatic and memory, contributions of the hippocampal system, particularly during hippocampal sharp-wave ripples.

Keyword(s): allostasis, body control, glucose regulation, hippocampus, homeostasis, memory, sharp-wave ripples
Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-101222-110632
2023-07-10
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/neuro/46/1/annurev-neuro-101222-110632.html?itemId=/content/journals/10.1146/annurev-neuro-101222-110632&mimeType=html&fmt=ahah

Literature Cited

  1. Alford FP, Baker HWG, Burger HG, de Kretser DM, Hudson B et al. 1973. Temporal patterns of integrated plasma hormone levels during sleep and wakefulness. I. Thyroid-stimulating hormone, growth hormone and cortisol. J. Clin. Endocrinol. Metab. 37:841–47
     [Google Scholar]
  2. Alonge KM, D'Alessio DA, Schwartz MW. 2021. Brain control of blood glucose levels: implications for the pathogenesis of type 2 diabetes. Diabetologia 64:5–14
     [Google Scholar]
  3. Anothaisintawee T, Reutrakul S, Van Cauter E, Thakkinstian A. 2016. Sleep disturbances compared to traditional risk factors for diabetes development: systematic review and meta-analysis. Sleep Med. Rev. 30:11–24
     [Google Scholar]
  4. Anthony TE, Dee N, Bernard A, Lerchner W, Heintz N, Anderson DJ. 2014. Control of stress-induced persistent anxiety by an extra-amygdala septohypothalamic circuit. Cell 156:522–36
     [Google Scholar]
  5. Antle MC, Silver R. 2005. Orchestrating time: arrangements of the brain circadian clock. Trends Neurosci. 28:145–51
     [Google Scholar]
  6. Antunes VR, Brailoiu GC, Kwok EH, Scruggs P, Dun NJ. 2001. Orexins/hypocretins excite rat sympathetic preganglionic neurons in vivo and in vitro. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281:R1801–7
     [Google Scholar]
  7. Åström K, Albertos P, Blanke M, Isidori A, Schaufelberger W, Sanz R, eds. 2001. Control of Complex Systems London: Springer-Verlag
  8. Banks WA, Kastin AJ. 1998. Differential permeability of the blood-brain barrier to two pancreatic peptides: insulin and amylin. Peptides 19:883–89
     [Google Scholar]
  9. Besedovsky HO, Del Rey AE, Sorkin E 1983. What do the immune system and the brain know about each other?. Immunol. Today 4:342–46
     [Google Scholar]
  10. Bohus B. 1961. The effect of central nervous lesions on pituitary-adrenocortical function in the rat. Acta Physiol. Acad. Sci. Hung. 20:373–77
     [Google Scholar]
  11. Bornstein SR. 1999. Adrenocorticotropin (ACTH)- and non-ACTH-mediated regulation of the adrenal cortex: neural and immune inputs. J. Clin. Endocrinol. Metab. 84:1729–36
     [Google Scholar]
  12. Brooks RA. 1991. Intelligence without representation. Artif. Intell. 47:139–59
     [Google Scholar]
  13. Buchanan TW, Tranel D, Kirschbaum C. 2009. Hippocampal damage abolishes the cortisol response to psychosocial stress in humans. Horm. Behav. 56:44–50
     [Google Scholar]
  14. Buzsáki G. 2013. Time, space and memory. Nature 497:568–69
     [Google Scholar]
  15. Buzsáki G. 2015. Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus 25:1073–188
     [Google Scholar]
  16. Buzsáki G. 2019. The Brain from Inside Out New York: Oxford Univ. Press
  17. Buzsáki G, McKenzie S, Davachi L. 2022. Neurophysiology of remembering. Annu. Rev. Psychol. 73:187–215
     [Google Scholar]
  18. Buzsáki G, Moser EI. 2013. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16:130–38
     [Google Scholar]
  19. Buzsáki G, Tingley D. 2018. Space and time: the hippocampus as a sequence generator. Trends Cogn. Sci. 22:853–69
     [Google Scholar]
  20. Chalmers DJ. 1997. The Conscious Mind: In Search of a Fundamental Theory New York: Oxford Univ. Press
  21. Chang H. 2007. Inventing Temperature: Measurement and Scientific Progress New York: Oxford Univ. Press
  22. Cisek P, Hayden BY. 2022. Neuroscience needs evolution. Philos. Trans. R. Soc. B 377:20200518
     [Google Scholar]
  23. Clark A. 1997. Being There: Putting Brain, Body, and World Together Again Cambridge, MA: MIT Press
  24. Craik FIM, Lockhart RS. 1972. Levels of processing: a framework for memory research. J. Verbal Learn. Verbal Behav. 11:671–84
     [Google Scholar]
  25. Cryan JF, O'Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS et al. 2019. The microbiota-gut-brain axis. Physiol. Rev. 99:1877–2013
     [Google Scholar]
  26. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW 2008. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9:46–56
     [Google Scholar]
  27. Diba K, Buzsáki G. 2007. Forward and reverse hippocampal place-cell sequences during ripples. Nat. Neurosci. 10:101241–42
     [Google Scholar]
  28. Dragoi G, Tonegawa S. 2011. Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469:397–401
     [Google Scholar]
  29. Eichenbaum H. 2004. Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44:109–20
     [Google Scholar]
  30. Frankland PW, Bontempi B. 2005. The organization of recent and remote memories. Nat. Rev. Neurosci. 6:119–30
     [Google Scholar]
  31. Friedman JM, Halaas JL. 1998. Leptin and the regulation of body weight in mammals. Nature 395:763–70
     [Google Scholar]
  32. Fuller PM, Gooley JJ, Saper CB. 2006. Neurobiology of the sleep-wake cycle: sleep architecture, circadian regulation, and regulatory feedback. J. Biol. Rhythms 21:482–93
     [Google Scholar]
  33. Gibbs J, Raymond W 2005. Embodiment and Cognitive Science Cambridge, UK: Cambridge Univ. Press
  34. Gibson J. 1966. The Senses Considered as Perceptual Systems Westport, CN: Praeger Revised ed .
  35. Gold PE. 1986. Glucose modulation of memory storage processing. Behav. Neural Biol. 45:342–49
     [Google Scholar]
  36. Gomez-Marin A, Ghazanfar AA. 2019. The life of behavior. Neuron 104:25–36
     [Google Scholar]
  37. González JA, Jensen LT, Iordanidou P, Strom M, Fugger L, Burdakov D. 2016. Inhibitory interplay between orexin neurons and eating. Curr. Biol. 26:2486–91
     [Google Scholar]
  38. Hafting T, Fyhn M, Molden S, Moser M-B, Moser EI. 2005. Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–6
     [Google Scholar]
  39. Hara J, Beuckmann CT, Nambu T, Willie JT, Chemelli RM et al. 2001. Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity. Neuron 30:345–54
     [Google Scholar]
  40. Harvey J, Solovyova N, Irving A. 2006. Leptin and its role in hippocampal synaptic plasticity. Prog. Lipid Res. 45:369–78
     [Google Scholar]
  41. Hegarty M, Waller D. 2004. A dissociation between mental rotation and perspective-taking spatial abilities. Intelligence 32:175–91
     [Google Scholar]
  42. Hsu TM, Hahn JD, Konanur VR, Noble EE, Suarez AN et al. 2015. Hippocampus ghrelin signaling mediates appetite through lateral hypothalamic orexin pathways. eLife 4:e11190
     [Google Scholar]
  43. Hubbard JI. 1974. The Peripheral Nervous System New York: Plenum Press
  44. Huszár R, Zhang Y, Blockus H, Buzsáki G. 2022. Preconfigured dynamics in the hippocampus are guided by embryonic birthdate and rate of neurogenesis. Nat. Neurosci. 25:1201–12
     [Google Scholar]
  45. Kanoski SE, Grill HJ. 2017. Hippocampus contributions to food intake control: mnemonic, neuroanatomical, and endocrine mechanisms. Biol. Psychiatry 81:748–56
     [Google Scholar]
  46. Karemaker JM. 2017. An introduction into autonomic nervous function. Physiol. Meas. 38:R89–118
     [Google Scholar]
  47. Kawakami N, Takatsuka N, Shimizu H. 2004. Sleep disturbance and onset of type 2 diabetes. Diabetes Care 27:282–83
     [Google Scholar]
  48. Kim SH, Park MJ. 2017. Effects of growth hormone on glucose metabolism and insulin resistance in human. Ann. Pediatr. Endocrinol. Metab. 22:145–52
     [Google Scholar]
  49. Kim C, Kim S, Park S. 2017. Neurogenic effects of ghrelin on the hippocampus. Int. J. Mol. Sci. 18:588
     [Google Scholar]
  50. Korol DL, Gold PE. 1998. Glucose, memory, and aging. Am. J. Clin. Nutr. 67:764S–71S
     [Google Scholar]
  51. Kuo T, McQueen A, Chen TC, Wang JC. 2015. Regulation of glucose homeostasis by glucocorticoids. Adv. Exp. Med. Biol. 872:99–126
     [Google Scholar]
  52. Lang D, Matthews D, Peto J, Turner R. 1979. Cyclic oscillations of basal plasma glucose and insulin concentration in human beings. N. Engl. J. Med. 301:1023–27
     [Google Scholar]
  53. Lathe R. 2001. Hormones and the hippocampus. J. Endocrinol. 169:205–31
     [Google Scholar]
  54. LeDoux J. 2022. As soon as there was life, there was danger: the deep history of survival behaviours and the shallower history of consciousness. Philos. Trans. R. Soc. B 377:20210292
     [Google Scholar]
  55. Levenstein D, Gornet J, Huszár R, Girardeau G, Grosmark A et al. 2022. Distinct ground state and activated state modes of firing in forebrain neurons. bioRxiv 2021.09.20.461152. https://doi.org/10.1101/2021.09.20.461152
  56. Llinás RR. 2002. I of the Vortex: From Neurons to Self Cambridge, MA: Bradford Books
  57. Luo L, Callaway EM, Svoboda K. 2008. Genetic dissection of neural circuits. Neuron 57:634–60
     [Google Scholar]
  58. Marr D. 1982. Vision: A Computational Investigation into the Human Representation and Processing of Visual Information Cambridge, MA: MIT Press
  59. McCormick DA, Nestvogel DB, He BJ. 2020. Neuromodulation of brain state and behavior. Annu. Rev. Neurosci. 43:391–415
     [Google Scholar]
  60. McEwen BS. 2007. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 87:873–904
     [Google Scholar]
  61. McNaughton BL, Barnes CA, Gerrard JL, Gothard K, Jung MW et al. 1996. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J. Exp. Biol. 199:173–85
     [Google Scholar]
  62. McNay EC, McCarty RC, Gold PE. 2001. Fluctuation in brain glucose concentration during behavioral testing: dissociations between brain areas and between brain and blood. Neurobiol. Learn. Mem. 75:325–37
     [Google Scholar]
  63. Mirzadeh Z, Faber CL, Schwartz MW. 2022. Central nervous system control of glucose homeostasis: a therapeutic target for type 2 diabetes?. Annu. Rev. Pharmacol. Toxicol. 62:55–84
     [Google Scholar]
  64. Mitchell KJ. 2020. Innate: How the Wiring of Our Brains Shapes Who We Are Princeton, NJ: Princeton Univ. Press
  65. Morais LH, Schreiber HL, Mazmanian SK. 2021. The gut microbiota-brain axis in behaviour and brain disorders. Nat. Rev. Microbiol. 19:241–55
     [Google Scholar]
  66. Neisser U. 1976. Cognition and Reality: Principles and Implications of Cognitive Psychology New York: WH Freeman and Co.
  67. Niell CM, Stryker MP. 2010. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65:472–79
     [Google Scholar]
  68. Niijima A. 1986. Neural control of blood glucose level. Jpn. J. Physiol. 36:827–41
     [Google Scholar]
  69. Northoff G. 2018. The Spontaneous Brain: From the Mind-Body to the World-Brain Problem Cambridge, MA: MIT Press
  70. O'Connell RG, Kelly SP 2021. Neurophysiology of human perceptual decision-making. Annu. Rev. Neurosci. 44:495–516
     [Google Scholar]
  71. O'Keefe J, Burgess N. 1996. Geometric determinants of the place fields of hippocampal neurons. Nature 381:425–28
     [Google Scholar]
  72. O'Keefe J, Nadel L. 1978. The Hippocampus as a Cognitive Map Oxford, UK: Oxford Univ. Press
  73. O'Malley D, MacDonald N, Mizielinska S, Connolly CN, Irving AJ, Harvey J. 2007. Leptin promotes rapid dynamic changes in hippocampal dendritic morphology. Mol. Cell. Neurosci. 35:559–72
     [Google Scholar]
  74. Parker PRL, Brown MA, Smear MC, Niell CM. 2020. Movement-related signals in sensory areas: roles in natural behavior. Trends Neurosci. 43:581–95
     [Google Scholar]
  75. Passingham RE, Stephan KE, Kötter R. 2002. The anatomical basis of functional localization in the cortex. Nat. Rev. Neurosci. 3:606–16
     [Google Scholar]
  76. Pastalkova E, Itskov V, Amarasingham A, Buzsáki G. 2008. Internally generated cell assembly sequences in the rat hippocampus. Science 321:1322–27
     [Google Scholar]
  77. Patterson JC, Ungerleider LG, Bandettini PA. 2002. Task-independent functional brain activity correlation with skin conductance changes: an fMRI study. NeuroImage 17:1797–806
     [Google Scholar]
  78. Pearson-Leary J, Jahagirdar V, Sage J, McNay EC. 2018. Insulin modulates hippocampally-mediated spatial working memory via glucose transporter-4. Behav. Brain Res. 338:32–39
     [Google Scholar]
  79. Plihal W, Born J. 1999. Memory consolidation in human sleep depends on inhibition of glucocorticoid release. NeuroReport 10:2741–47
     [Google Scholar]
  80. Pørksen N. 2002. The in vivo regulation of pulsatile insulin secretion. Diabetologia 45:3–20
     [Google Scholar]
  81. Quiroga RQ, Reddy L, Kreiman G, Koch C, Fried I. 2005. Invariant visual representation by single neurons in the human brain. Nature 435:1102–7
     [Google Scholar]
  82. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. 2001. A default mode of brain function. PNAS 98:676–82
     [Google Scholar]
  83. Rao RPN, Ballard DH. 1999. Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat. Neurosci. 2:79–87
     [Google Scholar]
  84. Rubin RT, Mandel AJ, Crandall PH. 1967. Corticosteroid responses to limbic stimulation in man: localization of stimulus sites. Science 153:767–68
     [Google Scholar]
  85. Schulingkamp RJ, Pagano TC, Hung D, Raffa RB 2000. Insulin receptors and insulin action in the brain: review and clinical implications. Neurosci. Biobehav. Rev. 24:855–72
     [Google Scholar]
  86. Seto K, Saito H, Otsuka K, Kawakami M. 1983. Influence of electrical stimulation of the limbic structure on insulin level in rabbit's plasma. Exp. Clin. Endocrinol. 89:347–49
     [Google Scholar]
  87. Sharma S, Kavuru M. 2010. Sleep and metabolism: an overview. Int. J. Endocrinol. 2010:270832
     [Google Scholar]
  88. Shein-Idelson M, Ondracek JM, Liaw H-P, Reiter S, Laurent G. 2016. Slow waves, sharp waves, ripples, and REM in sleeping dragons. Science 352:590–95
     [Google Scholar]
  89. Shigeo N, Seino Y, Ishida H, Seno M, Taminato T et al. 1987. Vagal regulation of insulin, glucagon, and somatostatin secretion in vitro in the rat. J. Clin. Investig. 79:1191–96
     [Google Scholar]
  90. Shimazu T. 1987. Neuronal regulation of hepatic glucose metabolism in mammals. Diabetes. Metab. Rev. 3:185–206
     [Google Scholar]
  91. Sloviter RS, Valiquette G, Abrams GM, Ronk EC, Sollas AL et al. 1989. Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science 243:535–38
     [Google Scholar]
  92. Slusher MA, Hyde JE. 1961. Inhibition of adrenal corticosteroid release by brain stem stimulation in cats1. Endocrinology 68:773–82
     [Google Scholar]
  93. Smarr BL, Jennings KJ, Driscoll JR, Kriegsfeld LJ. 2014. A time to remember: the role of circadian clocks in learning and memory. Behav. Neurosci. 128:283–303
     [Google Scholar]
  94. Sperry RW. 1950. Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43:482–89
     [Google Scholar]
  95. Sterling P, Eyer J 1988. Allostasis: a new paradigm to explain arousal pathology. Handbook of Life Stress, Cognition and Health S Fisher, J Reason 629–49. Oxford, UK: John Wiley & Sons
     [Google Scholar]
  96. Striedter G, Northcutt G. 2020. Brains Through Time: A Natural History of Vertebrates New York: Oxford Univ. Press
  97. Swanson RA, Levenstein D, McClain K, Tingley D, Buzsáki G. 2020. Variable specificity of memory trace reactivation during hippocampal sharp wave ripples. Curr. Opin. Behav. Sci. 32:126–35
     [Google Scholar]
  98. Tasali E, Leproult R, Ehrmann DA, Van Cauter E. 2008. Slow-wave sleep and the risk of type 2 diabetes in humans. PNAS 105:1044–49
     [Google Scholar]
  99. Taubøll E, Sveberg L, Svalheim S. 2015. Interactions between hormones and epilepsy. Seizure 28:3–11
     [Google Scholar]
  100. Tingley D, Buzsáki G. 2020. Routing of hippocampal ripples to subcortical structures via the lateral septum. Neuron 105:138–49.e5
     [Google Scholar]
  101. Tingley D, McClain K, Kaya E, Carpenter J, Buzsáki G. 2021. A metabolic function of the hippocampal sharp wave-ripple. Nature 597:82–86
     [Google Scholar]
  102. Tulving E. 2002. Episodic memory: from mind to brain. Annu. Rev. Psychol. 53:1–25
     [Google Scholar]
  103. Unger J, McNeill TH, Moxley RT, White M, Moss A, Livingston JN. 1989. Distribution of insulin receptor-like immunoreactivity in the rat forebrain. Neuroscience 31:143–57
     [Google Scholar]
  104. Vanderwolf CH. 1969. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26:407–18
     [Google Scholar]
  105. Vanderwolf CH, Stewart DJ. 1986. Joint cholinergic-serotonergic control of neocortical and hippocampal electrical activity in relation to behavior: effects of scopolamine, ditran, trifluoperazine and amphetamine. Physiol. Behav. 38:57–65
     [Google Scholar]
  106. Vargas R, Thorsteinsson H, Karlsson KAE. 2012. Spontaneous neural activity of the anterodorsal lobe and entopeduncular nucleus in adult zebrafish: a putative homologue of hippocampal sharp waves. Behav. Brain Res. 229:10–20
     [Google Scholar]
  107. von Holst E, Mittelstaedt H. 1950. Das Reafferenzprinzip. Naturwissenschaften 37:464–76
     [Google Scholar]
  108. Watson BO, Levenstein D, Greene JP, Gelinas JN, Buzsáki G. 2016. Network homeostasis and state dynamics of neocortical sleep. Neuron 90:839–52
     [Google Scholar]
  109. Wehrwein EA, Orer HS, Barman SM. 2016. Overview of the anatomy, physiology, and pharmacology of the autonomic nervous system. Compr. Physiol. 6:1239–78
     [Google Scholar]
  110. Wilson MA, McNaughton BL. 1994. Reactivation of hippocampal ensemble memories during sleep. Science 265:676–79
     [Google Scholar]
  111. Wolpert DM, Ghahramani Z, Jordan MI. 1995. An internal model for sensorimotor integration. Science 269:1880–82
     [Google Scholar]
  112. Yao Y, Barger Z, Doost MS, Tso CF, Darmohray D et al. 2022. Cardiovascular baroreflex circuit moonlights in sleep control. Neuron 110:3986–99.e6
     [Google Scholar]
  113. Zhang M, Fendler B, Peercy B, Goel P, Bertram R et al. 2008. Long lasting synchronization of calcium oscillations by cholinergic stimulation in isolated pancreatic islets. Biophys. J. 95:4676–88
     [Google Scholar]
/content/journals/10.1146/annurev-neuro-101222-110632
Loading
Cognition from the Body-Brain Partnership: Exaptation of Memory
Annual Review of Neuroscience 46, 191 (2023); https://doi.org/10.1146/annurev-neuro-101222-110632
/content/journals/10.1146/annurev-neuro-101222-110632
/content/journals/10.1146/annurev-neuro-101222-110632
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error