Do Teleost Fishes Possess a Homolog of Mammalian Isocortex?

Northcutt, R. Glenn

doi:10.1159/000330830

Cited by 43 publications

(41 citation statements)

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“…The finding that archer fish, a nonprimate species, have similar reflexive attentional processes, namely, facilitation and IOR (20), suggests these attentional processes in humans have an evolutionary ancestor. Fish lack laminated and columnar neural organization (21,22), visual cortex, and frontal and parietal cortical regions (which in humans are thought to guide volitional orienting). However, the fish does possess an optic tectum, which implies that subcortical mechanisms are probably involved in these types of reflexive processes.…”

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confidence: 99%

Endogenous orienting in the archer fish

Saban

Sekely

Klein

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The literature has long emphasized the neocortex's role in volitional processes. In this work, we examined endogenous orienting in an evolutionarily older species, the archer fish, which lacks neocortexlike cells. We used Posner's classic endogenous cuing task, in which a centrally presented, spatially informative cue is followed by a target. The fish responded to the target by shooting a stream of water at it. Interestingly, the fish demonstrated a human-like "volitional" facilitation effect: their reaction times to targets that appeared on the side indicated by the precue were faster than their reaction times to targets on the opposite side. The fish also exhibited inhibition of return, an aftermath of orienting that commonly emerges only in reflexive orienting tasks in human participants. We believe that this pattern demonstrates the acquisition of an arbitrary connection between spatial orienting and a nonspatial feature of a centrally presented stimulus in nonprimate species. In the literature on human attention, orienting in response to such contingencies has been strongly associated with volitional control. We discuss the implications of these results for the evolution of orienting, and for the study of volitional processes in all species, including humans.volitional orienting | subcortical regions | endogenous orienting | IOR | attention H umans are commonly assumed to have volitional abilities that species lacking a neocortex (e.g., fish and amphibians) do not have. The literature has long emphasized the role of cortical mechanisms in these exclusive cognitive abilities. But is a neocortex necessary for a species to manifest behaviors that have been attributed to volitional control? To examine this question, we tested whether the archer fish (Toxotes chatareus) is capable of endogenous orienting.Driven by bottom-up stimulation, reflexive orienting is fast and automatic as a result of tuning through natural selection. Volitional orienting is relatively nonreflexive and is tuned to local contingencies and/or the immediate goals of the individual (1). In the current study, we adopt the typical perspective regarding spatial attention, as put forward by Posner (2), which is characterized by two distinctions: whether covert or overt adjustments are made, and whether these adjustments are under endogenous (volitional) or exogenous (reflexive) control. The most common methods for examining reflexive and volitional attentional processes are two versions of Posner's cuing task (2, 3). In this task, participants are presented with a cue followed by a peripheral target to which they are instructed to respond. Two task properties are important for determining which mode of orienting is generated. The first is whether or not the cue is informative about the location of the upcoming target, and the second is whether or not the input pathway of the upcoming target might be stimulated by the cue. When studying reflexive orienting, the peripheral location where a target might appear, or one nearby, is stimulated by a cue...

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confidence: 99%

Endogenous orienting in the archer fish

Saban

Sekely

Klein

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…The large Dc neurons have been generally considered migrated components of the overlying pallial regions [Braford, 1995[Braford, , 2009Northcutt, 2006Northcutt, , 2008Northcutt, , 2011; however, Mueller et al [2011] provide evidence in zebrafish that Dc has a separate periventricular origin related to Dd. Northcutt [2011] points out that both of these origins may be valid depending on the species and subgroup of 'Dc' cells. This review concentrates on the 'dorsal' or largest Dc nucleus which is highly developed in the visually oriented percomorphs (Dcd; fig.…”

Section: The Teleost Palliummentioning

confidence: 99%

“…Concerning homologies of the teleost pallial areas with those of tetrapods, most of the evidence indicates that Dm represents the ventral pallium (pallial amygdala), Dl the medial pallium (hippocampus), and Dp the lateral pallium (olfactory cortex) [Braford, 1995[Braford, , 2009Northcutt, 2008Northcutt, , 2011Mueller and Wullimann, 2009]. Relationships of Dd and Dc to tetrapods remain unclear [Mueller et al, 2011;Northcutt, 2011].…”

Section: The Teleost Palliummentioning

confidence: 99%

“…Pallial Modulation of Lower Sensorimotor Centers Dc is characterized by several groups of mostly evenly distributed cells [Sheldon, 1912;Bannister, 1973;Northcutt and Braford, 1980;Demski and Beaver, 2001;Demski, 2003;Northcutt, 2006Northcutt, , 2011. The large neurons, which have long spiny dendrites with relatively few branches, are more or less spherical in the overall configuration ( fig.…”

Section: Dorsocentral Palliummentioning

confidence: 99%

“…The pallium, rather than other brain areas, is emphasized in this review for several reasons: (1) there is convincing evidence that the dorsolateral (Dl) and dorsomedial (Dm) regions of the teleost pallium are homologous to the tetrapod hippocampus and pallial amygdala respectively [Braford, 1995[Braford, , 2009Northcutt, 2006Northcutt, , 2008Northcutt, , 2011Mueller and Wullimann, 2009;Maximino et al, 2013], and that the homologous areas control similar aspects of cognition and emotion in both groups [Broglio et al, 2011]; (2) the two pallial areas and a related dorsocentral (Dc) region attain their greatest relative development in fishes with the most complex behaviors (see examples of large palliums in fig. 1 d, f-h) [Schroeder, 1980;Ridet and Bauchot, 1990;Demski and Beaver, 2001;Bshary et al, 2002;Demski, 2003;Bshary, 2011], and (3) Dl and Dm vary in their development in closely related species living in different physical and/or social environments [Shumway, 2008[Shumway, , 2010Park and Bell, 2010;Costa et al, 2011].…”

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The Pallium and Mind/Behavior Relationships in Teleost Fishes

Demski¹

2013

Brain Behav Evol

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Three interrelated pallial areas mediate behaviors reflective of the cognitive and emotional aspects of the teleost mind. The dorsocentral area (Dc) has specific associations with both of the other pallial areas and projects to major lower sensorimotor centers. While Dc generally functions as an output or modulatory component of the pallium, it probably also has integrative features important for certain behaviors. The dorsolateral region (Dl) has dorsal (Dld) and ventral (Dlv) divisions. In association with the dorsal part of Dc, Dld processes visual information via a ‘tectal loop' which is hypertrophied in certain coral reef species. The region also receives afferents related to other modalities. Functionally, Dld resembles the tetrapod sensory neocortex. Anatomical and behavioral data (i.e. involvement in spatial and temporal learning) strongly suggest that Dlv is homologous to the tetrapod hippocampus. The dorsal part of the dorsomedial area (Dmd) processes acoustic, lateral line, gustatory, and multimodal information. It has reciprocal connections with Dld such that the Dmd and Dld together can be considered the teleost nonolfactory ‘sensory pallium'. Behavioral studies indicate that Dmd creates the ‘fear' necessary for defense/escape and avoidance behaviors and controls several components of species-typical sexual and aggressive behavior (responsiveness, behavioral sequencing, and aspects of social cognition). While the functional results generally support the anatomical evidence that Dmd is homologous to the tetrapod amygdala, a case can also be made that Dmd has ‘sensory neocortex-like' features. Understanding the interrelationships of Dl, Dmd, and Dc seems a necessary ‘next step' in the identification of the neural processes responsible for mental experiences such as those of a unified sensory experience (Umwelt) or of feelings of discomfort versus well- being.

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Brain Evolution and Comparative Neuroanatomy

Powers¹

2014

Encyclopedia of Life Sciences

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Brains have many diverse forms in different animal groups, from complex layered structures to simple nerve nets. The range of different brain forms is reflective of the huge variety of environmental niches and lifestyles in which organisms have been successful. Both simple and elaborate brains are adaptive, depending on the selective pressures to which organisms are subjected. In vertebrates, a basic plan can be recognised across groups, especially in the brainstem, but the forebrain of birds and mammals is much more elaborate than those of other vertebrates. Elaborate nervous systems have developed independently in some molluscs, arthropods and vertebrates. Correlated with this elaboration is the capacity for complex learning, which is highly developed in some molluscs, arthropods and birds and mammals. The presence of elaborated brains in disparate groups illustrates that evolution of the brain has not shown a trend from simple to complex, but rather has occurred independently in different lineages. Key Concepts: Two structures are homologous if they can be traced to a common ancestor. Because brains do not fossilise, establishment of brain homologies requires as much information as possible about the similarities between brains of different groups. There is no trend in the evolution of the brain. Specialisations in brain traits develop in response to the demands of various environmental selective pressures. Many animals with simple nervous systems are very successful. Two major groups of invertebrates can be distinguished: those with radial symmetry and those with bilateral symmetry. Those with radial symmetry have simple nervous systems with a ring of neurons, while bilaterally symmetrical organisms have concentrations of neurons in the head region. Octopi, insects and crustaceans have elaborate brains, well‐developed eyes and extensive learning ability, rivalling that of mammals. The brains of the earliest chordate ancestors of vertebrates had bilateral eyes, a diencephalon and hindbrain. All vertebrates have the same subdivisions of the brain: the hindbrain, midbrain and forebrain (the diencephalon and telencephalon). The hindbrain is relatively conservative, retaining a recognisable structure in spite of many variations, whereas the forebrain shows more variability among vertebrate groups. Twenty‐five cranial nerves can be recognised in vertebrates, innervating muscles of the head and specialized sense organs, including lateral line organs and taste buds on the body surface. The vertebrate telencephalon includes a dorsal pallial area which differentiates into the cerebral cortex in mammals, but there is disagreement about the homologous areas in nonmammals. Brains have evolved to enable organisms to compete successfully in different environmental niches and the adaptations they show reflect the demands of those environments.

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Do Teleost Fishes Possess a Homolog of Mammalian Isocortex?

Cited by 43 publications

References 23 publications

Endogenous orienting in the archer fish

Endogenous orienting in the archer fish

The Pallium and Mind/Behavior Relationships in Teleost Fishes

Brain Evolution and Comparative Neuroanatomy

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