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Volumetric and connectivity assessment of the caudate nucleus in California sea lions and coyotes

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Abstract

In addition to a large (chimpanzee-sized) and heavily convoluted brain, one of the most striking neurobiological features in pinnipeds is the large size of the head of the caudate nucleus, which dwarfs the rest of the striatum. Although previous research has suggested carnivore striatum is small in comparison to that of primates, there are limited volumetric data on separate striatal structures in carnivores. Therefore, the apparent functional implication of a potentially hypertrophic caudate to carnivores has not been discussed. Here, for the first time, we obtained separate volumetric measurements of caudate and putamen in California sea lions and coyotes. Exemplars of both species had very large caudate nuclei, approximately 1/75th of total brain volume. In both the sea lion and coyote, the caudate dwarfed the putamen at a ratio of 13 to 1 or greater, a finding in strong contrast to measurements showing larger putamen than caudate in primates. In addition, using post-mortem diffusion tensor brain imaging, we mapped and compared white matter connections between the dorsal caudate and the motor, premotor and frontopolar, and orbitofrontal cortices in healthy adult sea lions and healthy adult coyotes. The sea lions showed some evidence of greater premotor and frontopolar connectivity. These findings bear on previously underexplored striatal characteristics of large carnivores, and we discuss potential interpretations related to cognitive flexibility and sensorimotor transformation.

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References

  • Abramson JZ, Hernández-Lloreda V, Call J, Colmenares F (2011) Relative quantity judgments in South American sea lions (Otaria flavescens). Anim Cogn 14(5):695

    Article  PubMed  Google Scholar 

  • Balleine BW, Delgado MR, Hikosaka O (2007) The role of the dorsal striatum in reward and decision making. J Neurosci 27(31):8161–8165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basser PJ, Mattiello J, LeBihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson Ser B 103(3):247–254

    Article  CAS  Google Scholar 

  • Bauer GB, Cook PF, Harley HE (2020) The relevance of ecological transitions to intelligence in marine mammals. Front Psychol 11

  • Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Smith SM (2003) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50(5):1077–1088

    Article  CAS  PubMed  Google Scholar 

  • Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? Neuroimage 34(1):144–155

    Article  CAS  PubMed  Google Scholar 

  • Berns GS, Brooks AM, Spivak M (2012) Functional MRI in awake unrestrained dogs. PLoS ONE 7(5):e38027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berns GS, Cook PF, Foxley S, Jbabdi S, Miller KL, Marino L (2015) Diffusion tensor imaging of dolphin brains reveals direct auditory pathway to temporal lobe. Proc R Soc b Biol Sci 282(1811):20151203

    Article  Google Scholar 

  • Bowyer RT (1987) Coyote group size relative to predation on mule deer

  • Buxton RB (1993) The diffusion sensitivity of fast steady-state free precession imaging. Magn Reson Med 29(2):235–243

    Article  CAS  PubMed  Google Scholar 

  • Campagna C, Harcourt R (eds) (2021) Ethology and behavioral ecology of Otariids and the Odobenid. Springer, New York

    Google Scholar 

  • Clarke HF, Robbins TW, Roberts AC (2008) Lesions of the medial striatum in monkeys produce perseverative impairments during reversal learning similar to those produced by lesions of the orbitofrontal cortex. J Neurosci 28(43):10972–10982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cook PF, Prichard A, Spivak M, Berns GS (2016) Awake canine fMRI predicts dogs’ preference for praise vs food. Soc Cogn Affect Neurosci 11(12):1853–1862

    PubMed  PubMed Central  Google Scholar 

  • Cook PF, Berns GS, Colegrove K, Johnson S, Gulland F (2018) Postmortem DTI reveals altered hippocampal connectivity in wild sea lions diagnosed with chronic toxicosis from algal exposure. J Comp Neurol 526(2):216–228

    Article  CAS  PubMed  Google Scholar 

  • Cook P, Reichmuth C, Hanke FD (2021) The mind of a Sea Lion. Ethology and behavioral ecology of Otariids and the Odobenid. Springer, Cham, pp 323–345

    Chapter  Google Scholar 

  • Cui DM, Yan YJ, Lynch JC (2003) Pursuit subregion of the frontal eye field projects to the caudate nucleus in monkeys. J Neurophysiol 89(5):2678–2684

    Article  PubMed  Google Scholar 

  • Dahlin E, Neely AS, Larsson A, Backman L, Nyberg L (2008) Transfer of learning after updating training mediated by the striatum. Science 320(5882):1510–1512

    Article  CAS  PubMed  Google Scholar 

  • Datta R, Lee J, Duda J, Avants BB, Vite CH, Tseng B, Aguirre GK (2012) A digital atlas of the dog brain. PLoS ONE 7(12):e52140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Roy T, Espinoza ER, Trillmich F (2021) Cooperation and opportunism in Galapagos sea lion hunting for shoaling fish. Ecol Evol 11(14):9206–9216

    Article  PubMed  PubMed Central  Google Scholar 

  • dos Santos LM, Ferro MM, Mota-Ortiz SR, Baldo MV, da Cunha C, Canteras NS (2007) Effects of ventrolateral striatal inactivation on predatory hunting. Physiol Behav 90(4):669–673

    Article  PubMed  Google Scholar 

  • Dunbar RI, Shultz S (2007) Understanding primate brain evolution. Philos Trans R Soc b Biol Sci 362(1480):649–658

    Article  CAS  Google Scholar 

  • Finkelstein A, Derdikman D, Rubin A, Foerster JN, Las L, Ulanovsky N (2015) Three-dimensional head-direction coding in the bat brain. Nature 517(7533):159–164

    Article  CAS  PubMed  Google Scholar 

  • Finlay BL, Darlington RB (1995) Linked regularities in the development and evolution of mammalian brains. Science 268(5217):1578–1584

    Article  CAS  PubMed  Google Scholar 

  • Flaherty AW, Graybiel AM (1993) Output architecture of the primate putamen. J Neurosci 13(8):3222–3237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fox KC, Muthukrishna M, Shultz S (2017) The social and cultural roots of whale and dolphin brains. Nat Ecol Evol 1(11):1699–1705

    Article  PubMed  Google Scholar 

  • Gahnstrom CJ, Spiers HJ (2020) Striatal and hippocampal contributions to flexible navigation in rats and humans. Brain Neurosci Adv 4:2398212820979772

    Article  PubMed  PubMed Central  Google Scholar 

  • Genty E, Roeder JJ (2006) Self-control: why should sea lions, Zalophus californianus, perform better than primates? Anim Behav 72(6):1241–1247

    Article  Google Scholar 

  • Ghahremani DG, Monterosso J, Jentsch JD, Bilder RM, Poldrack RA (2010) Neural components underlying behavioral flexibility in human reversal learning. Cereb Cortex 20(8):1843–1852

    Article  PubMed  Google Scholar 

  • Ghysen A (2003) The origin and evolution of the nervous system. Int J Dev Biol 47(7–8):555–562

    PubMed  Google Scholar 

  • Grahn JA, Parkinson JA, Owen AM (2008) The cognitive functions of the caudate nucleus. Prog Neurobiol 86(3):141–155

    Article  PubMed  Google Scholar 

  • Grisham W, Greta S, Schottler N, Tomita W, Burre A, Rostamian D, Thomas ST (2020) Brain volume fractions in mammals in relation to behavior in carnivores, primates, ungulates, and rodents. Brain Behav Evol 95(2):102–112

    Article  PubMed  Google Scholar 

  • Gutman DA, Keifer OP Jr, Magnuson ME, Choi DC, Majeed W, Keilholz S, Ressler KJ (2012) A DTI tractography analysis of infralimbic and prelimbic connectivity in the mouse using high-throughput MRI. Neuroimage 63(2):800–811

    Article  PubMed  Google Scholar 

  • Haruno M, Kawato M (2006) Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. J Neurophysiol 95(2):948–959

    Article  PubMed  Google Scholar 

  • Heiervang E, Behrens TEJ, Mackay CE, Robson MD, Johansen-Berg H (2006) Between session reproducibility and between subject variability of diffusion MR and tractography measures. Neuroimage 33(3):867–877

    Article  CAS  PubMed  Google Scholar 

  • Herculano-Houzel S (2019) Longevity and sexual maturity vary across species with number of cortical neurons, and humans are no exception. J Comp Neurol 527(10):1689–1705

    Article  PubMed  Google Scholar 

  • Herculano-Houzel S (2009) The human brain in numbers: a linearly scaled-up primate brain. Front Hum Neurosci 31

  • Hikosaka O, Sakamoto M, Usui S (1989) Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements. J Neurophysiol 61(4):780–798

    Article  CAS  PubMed  Google Scholar 

  • Hochner B (2013) How nervous systems evolve in relation to their embodiment: what we can learn from octopuses and other molluscs. Brain Behav Evol 82(1):19–30

    Article  PubMed  Google Scholar 

  • Iwaniuk AN (2010) Comparative brain collections are an indispensable resource for evolutionary neurobiology. Brain Behav Evol 76(2):87

    Article  PubMed  Google Scholar 

  • Jerison HJ (2019) Principles of the evolution of the brain and behavior. Evolution, Brain, and Behavior: Persistent Problems. Psychology Press, London, pp 23–45

    Chapter  Google Scholar 

  • Jürgens U (2002) Neural pathways underlying vocal control. Neurosci Biobehav Rev 26(2):235–258

    Article  PubMed  Google Scholar 

  • Kastak CR, Schusterman RJ, Kastak D (2001) Equivalence classification by California sea lions using class-specific reinforcers. J Exp Anal Behav 76(2):131–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimura M (1990) Behaviorally contingent property of movement-related activity of the primate putamen. J Neurophysiol 63(6):1277–1296

    Article  CAS  PubMed  Google Scholar 

  • Kirkby RJ (1969) Caudate nucleus lesions and perseverative behavior. Physiol Behav 4(4):451–454

    Article  Google Scholar 

  • Klanker M, Feenstra M, Denys D (2013) Dopaminergic control of cognitive flexibility in humans and animals. Front Neurosci 7:201

    Article  PubMed  PubMed Central  Google Scholar 

  • Lau B, Glimcher PW (2007) Action and outcome encoding in the primate caudate nucleus. J Neurosci 27(52):14502–14514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marino L (2004) Dolphin cognition. Curr Biol 14(21):R910–R911

    Article  CAS  PubMed  Google Scholar 

  • McKnight JC, Ruesch A, Bennett K, Bronkhorst M, Balfour S, Moss SE, Hastie GD (2021) Shining new light on sensory brain activation and physiological measurement in seals using wearable optical technology. Philos Trans R Soc B 376(1830):20200224

    Article  Google Scholar 

  • McNab JA, Jbabdi S, Deoni SC, Douaud G, Behrens TE, Miller KL (2009) High resolution diffusion-weighted imaging in fixed human brain using diffusion-weighted steady state free precession. Neuroimage 46(3):775–785

    Article  PubMed  Google Scholar 

  • Miller KL, Stagg CJ, Douaud G, Jbabdi S, Smith SM, Behrens TE, McNab JA (2011) Diffusion imaging of whole, post-mortem human brains on a clinical MRI scanner. Neuroimage 57(1):167–181

    Article  PubMed  Google Scholar 

  • Miller KL, McNab JA, Jbabdi S, Douaud G (2012) Diffusion tractography of post-mortem human brains: optimization and comparison of spin echo and steady-state free precession techniques. Neuroimage 59(3):2284–2297

    Article  PubMed  Google Scholar 

  • Montie EW, Pussini N, Schneider GE, Battey TW, Dennison S, Barakos J, Gulland F (2009) Neuroanatomy and volumes of brain structures of a live California sea lion (Zalophus californianus) from magnetic resonance images. Anat Record Adv Integr Anat Evol Biol Adv Integr Anat Evol Biol 292(10):1523–1547

    Article  Google Scholar 

  • Morgane PJ, Glezer II (1990) Sensory neocortex in dolphin brain. Sensory abilities of cetaceans. Springer, Boston, pp 107–136

    Chapter  Google Scholar 

  • Oelschläger HH (2008) The dolphin brain—a challenge for synthetic neurobiology. Brain Res Bull 75(2–4):450–459

    Article  PubMed  Google Scholar 

  • Postle BR, D’Esposito M (1999) Dissociation of human caudate nucleus activity in spatial and nonspatial working memory: an event-related fMRI study. Cogn Brain Res 8(2):107–115

    Article  CAS  Google Scholar 

  • Postle BR, D’Esposito M (2003) Spatial working memory activity of the caudate nucleus is sensitive to frame of reference. Cogn Affect Behav Neurosci 3(2):133–144

    Article  PubMed  Google Scholar 

  • Reep RL, Finlay BL, Darlington RB (2007) The limbic system in mammalian brain evolution. Brain Behav Evol 70(1):57–70

    Article  CAS  PubMed  Google Scholar 

  • Ridgway SH, Brownson RH, Van Alstyne KR, Hauser RA (2019) Higher neuron densities in the cerebral cortex and larger cerebellums may limit dive times of delphinids compared to deep-diving toothed whales. PLoS ONE 14(12):e0226206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rilling JK (2014) Comparative primate neuroimaging: insights into human brain evolution. Trends Cogn Sci 18(1):46–55

    Article  PubMed  Google Scholar 

  • Sato K, Aoki K, Watanabe YY, Miller PJ (2013) Neutral buoyancy is optimal to minimize the cost of transport in horizontally swimming seals. Sci Rep 3(1):1–5

    Article  Google Scholar 

  • Sawyer EK, Turner EC, Kaas JH (2016) Somatosensory brainstem, thalamus, and cortex of the California sea lion (Zalophus californianus). J Comp Neurol 524(9):1957–1975

    Article  PubMed  PubMed Central  Google Scholar 

  • Schusterman RJ, Kastak D (1993) A California sea lion (Zalophus californianus) is capable of forming equivalence relations. Psychol Record 43(4):823–839

    Article  Google Scholar 

  • Schusterman RJ, Kellogg WN, Rice CE (1965) Underwater visual discrimination by the California sea lion. Science 147(3665):1594–1596

    Article  CAS  PubMed  Google Scholar 

  • Schusterman RJ, Kastak CR, Kastak D (2002) The cognitive sea lion: Meaning and memory in the laboratory and in nature

  • Sea Lion Hunters (2013). https://www.youtube.com/watch?v=VX6XSqP6UVo

  • Sliwa J, Freiwald WA (2017) A dedicated network for social interaction processing in the primate brain. Science 356(6339):745–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sporns O (2007) Brain connectivity. Scholarpedia 2(10):4695

    Article  Google Scholar 

  • Travain T, Colombo ES, Grandi LC, Heinzl E, Pelosi A, Previde EP, Valsecchi P (2016) How good is this food? A study on dogs’ emotional responses to a potentially pleasant event using infrared thermography. Physiol Behav 159:80–87

    Article  CAS  PubMed  Google Scholar 

  • Van Bourg J, Young JK, Alkhalifah R, Brummer S, Johansson E, Morton J, Wynne CD (2022) Cognitive flexibility and aging in coyotes (Canis latrans). J Comp Psychol

  • Vonk J, Leete JA (2017) Carnivore concepts: categorization in carnivores “bears” further study. Int J Comp Psychol 30:1–22

    Article  Google Scholar 

  • Washington SD, Hamaide J, Jeurissen B, Van Steenkiste G, Huysmans T, Sijbers J, Verhoye M (2018) A three-dimensional digital neurological atlas of the mustached bat (Pteronotus parnellii). Neuroimage 183:300–313

    Article  PubMed  Google Scholar 

  • Whishaw IQ, O’Connor WT, Dunnett SB (1986) The contributions of motor cortex, nigrostriatal dopamine and caudate-putamen to skilled forelimb use in the rat. Brain 109(5):805–843

    Article  PubMed  Google Scholar 

  • Wilson RP, Griffiths IW, Mills MG, Carbone C, Wilson JW, Scantlebury DM (2015) Mass enhances speed but diminishes turn capacity in terrestrial pursuit predators. Elife 4:e06487

    Article  PubMed Central  Google Scholar 

  • Yeh FC, Verstynen TD, Wang Y, Fernández-Miranda JC, Tseng WYI (2013) Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS ONE 8(11):e80713

    Article  PubMed  PubMed Central  Google Scholar 

  • Yin D, Valles FE, Fiandaca MS, Forsayeth J, Larson P, Starr P, Bankiewicz KS (2009) Striatal volume differences between non-human and human primates. J Neurosci Methods 176(2):200–205

    Article  PubMed  Google Scholar 

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  1. New College of Florida, Sarasota, USA

    Peter F. Cook

  2. Emory University, Atlanta, USA

    Gregory Berns

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Cook, P.F., Berns, G. Volumetric and connectivity assessment of the caudate nucleus in California sea lions and coyotes. Anim Cogn 25, 1231–1240 (2022). https://doi.org/10.1007/s10071-022-01685-7

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