{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,7,30]],"date-time":"2025-07-30T16:16:00Z","timestamp":1753892160100,"version":"3.41.2"},"reference-count":64,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,10,3]],"date-time":"2023-10-03T00:00:00Z","timestamp":1696291200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Physiol."],"abstract":"<jats:p>Nervous systems of vertebrates and invertebrates show a common modular theme in the flow of information for cost-benefit decisions. Sensory inputs are incentivized by integrating stimulus qualities with motivation and memory to affect appetitive state, a system of homeostatic drives, and labelled for directionality. Appetitive state determines action responses from a repertory of possibles and transmits the decision to a premotor system that frames the selected action in motor arousal and appropriate postural and locomotion commands. These commands are then sent to the primary motor pattern generators controlling the motorneurons, with feedback at each stage. In the vertebrates, these stages are mediated by forebrain pallial derivatives for incentive and directionality (olfactory bulb, cerebral cortex, pallial amygdala, <jats:italic>etc.<\/jats:italic>) interacting with hypothalamus (homeostasis, motivation, and reward) for action selection in the forebrain basal ganglia, the mid\/hindbrain reticular formation as a premotor translator for posture, locomotion, and arousal state, and the spinal cord and cranial nuclei as primary motor pattern generators. Gastropods, like the predatory sea slug <jats:italic>Pleurobranchaea californica<\/jats:italic>, show a similar organization but with differences that suggest how complex brains evolved from an ancestral soft-bodied bilaterian along with segmentation, jointed skeletons, and complex exteroceptors. Their premotor feeding network combines functions of hypothalamus and basal ganglia for homeostasis, motivation, presumed reward, and action selection for stimulus approach or avoidance. In <jats:italic>Pleurobranchaea<\/jats:italic>, the premotor analogy to the vertebrate reticular formation is the bilateral \u201cA-cluster\u201d of cerebral ganglion neurons that controls posture, locomotion, and serotonergic motor arousal. The A-cluster transmits motor commands to the pedal ganglia analogs of the spinal cord, for primary patterned motor output. Apparent pallial precursors are not immediately evident in <jats:italic>Pleurobranchaea<\/jats:italic>\u2019s central nervous system, but a notable candidate is a subepithelial nerve net in the peripheral head region that integrates chemotactile stimuli for incentive and directionality. Evolutionary centralization of its computational functions may have led to the olfaction-derived pallial forebrain in the ancestor\u2019s vertebrate descendants and their analogs in arthropods and annelids.<\/jats:p>","DOI":"10.3389\/fphys.2023.1263453","type":"journal-article","created":{"date-parts":[[2023,10,5]],"date-time":"2023-10-05T03:49:16Z","timestamp":1696477756000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":2,"title":["A common modular design of nervous systems originating in soft-bodied invertebrates"],"prefix":"10.3389","volume":"14","author":[{"given":"Ekaterina D.","family":"Gribkova","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Colin A.","family":"Lee","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jeffrey W.","family":"Brown","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jilai","family":"Cui","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yichen","family":"Liu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tigran","family":"Norekian","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rhanor","family":"Gillette","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2023,10,3]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"402","DOI":"10.3389\/fnins.2015.00402","article-title":"Olfaction, navigation, and the origin of isocortex","volume":"9","author":"Aboitiz","year":"2015","journal-title":"Front. Neurosci."},{"key":"B2","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1017\/s0140525x03000128","article-title":"The evolutionary origin of the mammalian isocortex: towards an integrated developmental and functional approach","volume":"26","author":"Aboitiz","year":"2003","journal-title":"Behav. Brain Sci."},{"key":"B3","doi-asserted-by":"publisher","first-page":"1869","DOI":"10.4249\/scholarpedia.1869","article-title":"Modular models of brain function","volume":"2","author":"Arbib","year":"2007","journal-title":"Scholarpedia"},{"key":"B4","doi-asserted-by":"publisher","first-page":"579","DOI":"10.2307\/1416470","article-title":"Higher order conditioning","volume":"52","author":"Brogden","year":"1939","journal-title":"Am. J. Psychol."},{"key":"B5","unstructured":"BrownJ. W.\n          ChampaignUniversity of Illinois at Urbana-ChampaignReciprocal interactions between feeding and turning motor networks mediate foraging decisions in a predatory sea-slug2014"},{"key":"B6","doi-asserted-by":"publisher","first-page":"e0208891","DOI":"10.1371\/journal.pone.0208891","article-title":"A role for dopamine in the peripheral sensory processing of a gastropod mollusc","volume":"13","author":"Brown","year":"2018","journal-title":"PLOS One"},{"key":"B7","doi-asserted-by":"publisher","first-page":"104","DOI":"10.3389\/fendo.2017.00104","article-title":"Hunger and satiety gauge reward sensitivity","volume":"8","author":"Cassidy","year":"2017","journal-title":"Front. Endocrinol."},{"key":"B8","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1007\/978-3-030-78471-3_3","article-title":"Feeling, seeing, and liking: how bodily resources inform perception and emotion","volume-title":"Handbook of embodied psychology","author":"Clore","year":"2021"},{"key":"B9","first-page":"98","article-title":"Functional anatomy of olfactory sense organs","volume":"11","author":"Cuschieri","year":"1976","journal-title":"St. Luke's Hosp. Gazette"},{"key":"B10","doi-asserted-by":"publisher","first-page":"801","DOI":"10.1126\/science.622572","article-title":"Neural correlate of behavioral plasticity in command neurons of Pleurobranchaea","volume":"199","author":"Davis","year":"1978","journal-title":"Science"},{"key":"B11","doi-asserted-by":"publisher","first-page":"E5854","DOI":"10.1073\/pnas.1508422112","article-title":"Neural substrate for higher-order learning in an insect: mushroom bodies are necessary for configural discriminations","volume":"112","author":"Devaud","year":"2015","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B12","doi-asserted-by":"publisher","first-page":"1785","DOI":"10.1152\/jn.00005.2017","article-title":"The role of the hippocampus in navigation is memory","volume":"117","author":"Eichenbaum","year":"2017","journal-title":"J. Neurophysiology"},{"key":"B13","doi-asserted-by":"publisher","first-page":"877","DOI":"10.1242\/jeb.205.7.877","article-title":"Comparative neuroethology of feeding control in molluscs","volume":"205","author":"Elliott","year":"2002","journal-title":"J. Exp. Biol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1016\/j.virusres.2006.01.010","article-title":"The origin of viruses and their possible roles in major evolutionary transitions","volume":"117","author":"Forterre","year":"2006","journal-title":"Virus Res."},{"key":"B15","doi-asserted-by":"publisher","first-page":"1855","DOI":"10.1242\/jeb.202.14.1855","article-title":"Oscillatory dynamics and information processing in olfactory systems","volume":"202","author":"Gelperin","year":"1999","journal-title":"J. Exp. Biol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"1058","DOI":"10.1093\/icb\/icv081","article-title":"The sea slug, Pleurobranchaea californica: A signpost species in the evolution of complex nervous systems and behavior","volume":"55","author":"Gillette","year":"2015","journal-title":"Integr. Comp. Biol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1007\/bf00605400","article-title":"The role of the metacerebral giant neuron in the feeding behavior of Pleurobranchaea","volume":"116","author":"Gillette","year":"1977","journal-title":"J. Comp. Physiology"},{"key":"B18","doi-asserted-by":"publisher","first-page":"838","DOI":"10.1093\/icb\/icl024","article-title":"Evolution and function in serotonergic systems","volume":"46","author":"Gillette","year":"2006","journal-title":"Integr. Comp. Biol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"3585","DOI":"10.1073\/pnas.97.7.3585","article-title":"Cost-benefit analysis potential in feeding behavior of a predatory snail by integration of hunger, taste, and pain","volume":"97","author":"Gillette","year":"2000","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B20","doi-asserted-by":"publisher","first-page":"983","DOI":"10.1093\/icb\/41.4.983","article-title":"The role of the escape swim motor network in the organization of behavioral hierarchy and arousal in Pleurobranchaea","volume":"41","author":"Gillette","year":"2001","journal-title":"Am. Zoologist"},{"key":"B21","doi-asserted-by":"publisher","first-page":"234","DOI":"10.2307\/1542393","article-title":"On the significance of neuronal giantism in gastropods","volume":"180","author":"Gillette","year":"1991","journal-title":"Biol. Bull."},{"key":"B22","doi-asserted-by":"publisher","first-page":"9627","DOI":"10.1038\/s41598-020-66465-0","article-title":"Simple aesthetic sense and addiction emerge in neural relations of cost-benefit decision in foraging","volume":"10","author":"Gribkova","year":"2020","journal-title":"Sci. Rep."},{"key":"B23","doi-asserted-by":"publisher","first-page":"5425","DOI":"10.1113\/jphysiol.2012.246660","article-title":"The evolutionary origin of the vertebrate basal ganglia and its role in action selection","volume":"591","author":"Grillner","year":"2013","journal-title":"J. Physiol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"636","DOI":"10.1037\/\/0735-7044.112.3.636","article-title":"Classical conditioning, differential conditioning, and second-order conditioning of the Aplysia gill-withdrawal reflex in a simplified mantle organ preparation","volume":"112","author":"Hawkins","year":"1998","journal-title":"Behav. Neurosci."},{"key":"B25","doi-asserted-by":"publisher","first-page":"382","DOI":"10.1038\/nature07309","article-title":"Acoel development indicates the independent evolution of the bilaterian mouth and anus","volume":"456","author":"Hejnol","year":"2008","journal-title":"Nature"},{"key":"B26","doi-asserted-by":"publisher","first-page":"123","DOI":"10.3389\/fnins.2012.00123","article-title":"A core circuit module for cost\/benefit decision","volume":"6","author":"Hirayama","year":"2012","journal-title":"Front. Neurosci."},{"key":"B27","doi-asserted-by":"publisher","first-page":"118","DOI":"10.1016\/j.cub.2011.10.055","article-title":"A neuronal network switch for approach\/avoidance toggled by appetitive state","volume":"22","author":"Hirayama","year":"2012","journal-title":"Curr. Biol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"e102240","DOI":"10.1371\/journal.pone.0102240","article-title":"Neuromodulatory control of a goal-directed decision","volume":"9","author":"Hirayama","year":"2014","journal-title":"PLOS One"},{"key":"B29","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1159\/000353419","article-title":"How nervous systems evolve in relation to their embodiment: what we can learn from octopuses and other molluscs","volume":"82","author":"Hochner","year":"2013","journal-title":"Brain, Behav. Evol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"R146","DOI":"10.1016\/j.cub.2015.12.024","article-title":"Tunicates","volume":"26","author":"Holland","year":"2016","journal-title":"Curr. Biol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"10693","DOI":"10.1073\/pnas.1201880109","article-title":"From chemotaxis to the cognitive map: the function of olfaction","volume":"109","author":"Jacobs","year":"2012","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B32","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1007\/s10071-022-01734-1","article-title":"The PROUST hypothesis: the embodiment of olfactory cognition","volume":"26","author":"Jacobs","year":"2023","journal-title":"Anim. Cogn."},{"key":"B33","doi-asserted-by":"publisher","first-page":"654","DOI":"10.1152\/jn.1999.81.2.654","article-title":"Central pattern generator for escape swimming in the notaspid sea slug Pleurobranchaea californica","volume":"81","author":"Jing","year":"1999","journal-title":"J. Neurophysiology"},{"key":"B34","doi-asserted-by":"publisher","first-page":"3039","DOI":"10.1523\/JNEUROSCI.23-07-03039.2003","article-title":"Directional avoidance turns encoded by single interneurons and sustained by multifunctional serotonergic cells","volume":"23","author":"Jing","year":"2003","journal-title":"J. Neurosci."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1346","DOI":"10.1152\/jn.2000.83.3.1346","article-title":"Escape swim network interneurons have diverse roles in behavioral switching and putative arousal in Pleurobranchaea","volume":"83","author":"Jing","year":"2000","journal-title":"J. Neurophysiology"},{"key":"B36","doi-asserted-by":"publisher","first-page":"1900","DOI":"10.1152\/jn.1995.74.5.1900","article-title":"Neuronal elements that mediate escape swimming and suppress feeding behavior in the predatory sea slug Pleurobranchaea","volume":"74","author":"Jing","year":"1995","journal-title":"J. Neurophysiology"},{"key":"B37","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1515\/revneuro.2009.20.5-6.405","article-title":"Evolving concepts of arousal: insights from simple model systems","volume":"20","author":"Jing","year":"2009","journal-title":"Rev. Neurosci."},{"key":"B38","doi-asserted-by":"publisher","first-page":"12349","DOI":"10.1523\/JNEUROSCI.3855-08.2008","article-title":"Neural analog of arousal: persistent conditional activation of a feeding modulator by serotonergic initiators of locomotion","volume":"28","author":"Jing","year":"2008","journal-title":"J. Neurosci."},{"key":"B39","doi-asserted-by":"publisher","first-page":"374","DOI":"10.1152\/jn.2000.83.1.374","article-title":"Modulation of fictive feeding by dopamine and serotonin in Aplysia","volume":"83","author":"Kabotyanski","year":"2000","journal-title":"J. Neurophysiology"},{"key":"B40","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.conb.2016.07.004","article-title":"Phylogenetic plasticity in the evolution of molluscan neural circuits","volume":"41","author":"Katz","year":"2016","journal-title":"Curr. Opin. Neurobiol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1016\/j.conb.2014.10.004","article-title":"Olfactory system oscillations across phyla","volume":"31","author":"Kay","year":"2015","journal-title":"Curr. Opin. Neurobiol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/j.tins.2006.11.007","article-title":"An argument for an olfactory thalamus","volume":"30","author":"Kay","year":"2007","journal-title":"Trends Neurosci."},{"key":"B43","doi-asserted-by":"publisher","first-page":"3647","DOI":"10.1523\/JNEUROSCI.1386-22.2023","article-title":"Coordination of locomotion by serotonergic neurons in the predatory gastropod Pleurobranchaea californica","volume":"43","author":"Lee","year":"2023","journal-title":"J. Neurosci."},{"key":"B44","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1111\/j.1463-6395.2009.00422.x","article-title":"The mushroom bodies\u2013prominent brain centres of arthropods and annelids with enigmatic evolutionary origin","volume":"91","author":"Loesel","year":"2010","journal-title":"Acta Zool."},{"key":"B45","doi-asserted-by":"publisher","first-page":"4058","DOI":"10.1073\/pnas.83.11.4058","article-title":"Mechanism for food avoidance learning in the central pattern generator of feeding behavior of Pleurobranchae californica","volume":"83","author":"London","year":"1986","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B46","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1002\/(sici)1096-9861(19970602)382:2<176:aid-cne3>3.0.co;2-0","article-title":"Serotonin-immunoreactivity in peripheral tissues of the opisthobranch molluscs Pleurobranchaea californica and Tritonia diomedea","volume":"382","author":"Moroz","year":"1997","journal-title":"J. Comp. Neurology"},{"key":"B47","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1016\/j.pneurobio.2010.11.001","article-title":"Neuronal control of swimming behavior: comparison of vertebrate and invertebrate model systems","volume":"93","author":"Mullins","year":"2011","journal-title":"Prog. Neurobiol."},{"key":"B48","doi-asserted-by":"publisher","first-page":"3231","DOI":"10.1242\/jeb.079384","article-title":"Selective prey avoidance learning in the predatory sea-slug Pleurobranchaea californica","volume":"216","author":"Noboa","year":"2013","journal-title":"J. Exp. Biol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"1985","DOI":"10.1523\/JNEUROSCI.22-05-01985.2002","article-title":"Highly dissimilar behaviors mediated by a multifunctional network in the marine mollusk Tritonia diomedea","volume":"22","author":"Popescu","year":"2002","journal-title":"J. Neurosci."},{"key":"B50","doi-asserted-by":"publisher","first-page":"1009","DOI":"10.1016\/S0306-4522(98)00319-4","article-title":"The basal ganglia: a vertebrate solution to the selection problem?","volume":"89","author":"Redgrave","year":"1999","journal-title":"Neuroscience"},{"key":"B51","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1016\/s0165-0173(98)00016-2","article-title":"Structural and functional evolution of the basal ganglia in vertebrates","volume":"28","author":"Reiner","year":"1998","journal-title":"Brain Res. Rev."},{"key":"B52","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1152\/physrev.00028.2005","article-title":"Dynamic sensorimotor interactions in locomotion","volume":"86","author":"Rossignol","year":"2006","journal-title":"Physiol. Rev."},{"key":"B53","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1046\/j.1469-7580.2000.19640501.x","article-title":"Evolution of the basal ganglia: new perspectives through a comparative approach","volume":"196","author":"Smeets","year":"2000","journal-title":"J. Anat."},{"key":"B54","doi-asserted-by":"publisher","first-page":"634","DOI":"10.1016\/S0959-4388(99)00019-7","article-title":"Olfactory systems: common design, uncommon origins?","volume":"9","author":"Strausfeld","year":"1999","journal-title":"Curr. Opin. Neurobiol."},{"key":"B55","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1126\/science.1231828","article-title":"Deep homology of arthropod central complex and vertebrate basal ganglia","volume":"340","author":"Strausfeld","year":"2013","journal-title":"Science"},{"key":"B56","doi-asserted-by":"publisher","first-page":"466","DOI":"10.1002\/(sici)1096-9861(19980615)395:4<466:aid-cne4>3.0.co;2-#","article-title":"Serotonin immunoreactivity in the central nervous system of the marine molluscs Pleurobranchaea californica and Tritonia diomedea","volume":"395","author":"Sudlow","year":"1998","journal-title":"J. Comp. Neurology"},{"key":"B57","doi-asserted-by":"publisher","first-page":"1965","DOI":"10.1016\/j.celrep.2015.10.061","article-title":"Activity of raph\u00e9 serotonergic neurons controls emotional behaviors","volume":"13","author":"Teissier","year":"2015","journal-title":"Cell Rep."},{"key":"B58","doi-asserted-by":"publisher","first-page":"800","DOI":"10.1016\/j.cell.2010.07.043","article-title":"Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium","volume":"142","author":"Tomer","year":"2010","journal-title":"Cell"},{"key":"B59","doi-asserted-by":"publisher","first-page":"1080","DOI":"10.1016\/j.conb.2013.09.005","article-title":"The bilaterian forebrain: an evolutionary chimaera","volume":"23","author":"Tosches","year":"2013","journal-title":"Curr. Opin. Neurobiol."},{"key":"B60","doi-asserted-by":"publisher","first-page":"704","DOI":"10.1016\/j.conb.2010.08.022","article-title":"Basal ganglia contributions to motor control: a vigorous tutor","volume":"20","author":"Turner","year":"2010","journal-title":"Curr. Opin. Neurobiol."},{"key":"B61","doi-asserted-by":"publisher","first-page":"15","DOI":"10.3389\/fnana.2017.00015","article-title":"The brainstem in emotion: a review","volume":"11","author":"Venkatraman","year":"2017","journal-title":"Front. Neuroanat."},{"key":"B62","doi-asserted-by":"publisher","first-page":"5878","DOI":"10.1073\/pnas.1610602114","article-title":"Whole-organism cellular gene-expression atlas reveals conserved cell types in the ventral nerve cord of Platynereis dumerilii","volume":"114","author":"Vergara","year":"2017","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B63","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1242\/jeb.02697","article-title":"Orienting and avoidance turning are precisely computed by the predatory sea-slug Pleurobranchaea californica McFarland","volume":"210","author":"Yafremava","year":"2007","journal-title":"J. Exp. Biol."},{"key":"B64","doi-asserted-by":"publisher","first-page":"2885","DOI":"10.1152\/jn.00124.2011","article-title":"Putative lateral inhibition in sensory processing for directional turns","volume":"105","author":"Yafremava","year":"2011","journal-title":"J. Neurophysiology"}],"container-title":["Frontiers in Physiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2023.1263453\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,5]],"date-time":"2023-10-05T03:49:19Z","timestamp":1696477759000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2023.1263453\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,10,3]]},"references-count":64,"alternative-id":["10.3389\/fphys.2023.1263453"],"URL":"https:\/\/doi.org\/10.3389\/fphys.2023.1263453","relation":{},"ISSN":["1664-042X"],"issn-type":[{"type":"electronic","value":"1664-042X"}],"subject":[],"published":{"date-parts":[[2023,10,3]]},"article-number":"1263453"}}