Comparative morphology of three types of projection‐identified pyramidal neurons in the superficial layers of cat visual cortex

Matsubara, Joanne A.; Chase, Ronald; Thejomayen, Moira

doi:10.1002/(sici)1096-9861(19960226)366:1<93::aid-cne7>3.3.co;2-h

Cited by 11 publications

(15 citation statements)

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“…Thus, it is tempting to conclude that highly complex pyramidal cells in the dorsolateral gPFC is a characteristic of the latter species, which may differ from that in other primates that diverged earlier, such as New World monkeys and the great apes. Alternatively, the apparent species differences may reflect regional variation in neuronal maturation rates (Jacobs and Scheibel, 1993; Jacobs et al, 1995, 1997; Page et al, 2002; Duan et al, 2003; Elston et al, 2009, 2010a,b) or arise through sampling different subsets of projection neurons in the different cortical areas, which have been shown to differ in both their morphology (Schofield et al, 1987; Hallman et al, 1988; Hübener and Bolz, 1988; de Lima et al, 1990; Hübener et al, 1990; Einstein, 1996; Matsubara et al, 1996; Duan et al, 2002; Soloway et al, 2002; Elston and Rosa, 2006) and density (Jones and Powell, 1970; Barbas, 1992; Young, 1992; Pandya and Yeterian, 2000; Petrides, 2000; Collins et al, 2005) in different cortical areas. In either case, the result is consistent with our main conclusion that pyramidal cells develop differently among cortical areas and mature into specialized circuits.…”

Section: Discussionmentioning

confidence: 99%

Pyramidal cells in prefrontal cortex of primates: marked differences in neuronal structure among species

Elston¹,

Benavides-Piccione

Elston³

et al. 2011

Front. Neuroanat.

105

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The most ubiquitous neuron in the cerebral cortex, the pyramidal cell, is characterized by markedly different dendritic structure among different cortical areas. The complex pyramidal cell phenotype in granular prefrontal cortex (gPFC) of higher primates endows specific biophysical properties and patterns of connectivity, which differ from those in other cortical regions. However, within the gPFC, data have been sampled from only a select few cortical areas. The gPFC of species such as human and macaque monkey includes more than 10 cortical areas. It remains unknown as to what degree pyramidal cell structure may vary among these cortical areas. Here we undertook a survey of pyramidal cells in the dorsolateral, medial, and orbital gPFC of cercopithecid primates. We found marked heterogeneity in pyramidal cell structure within and between these regions. Moreover, trends for gradients in neuronal complexity varied among species. As the structure of neurons determines their computational abilities, memory storage capacity and connectivity, we propose that these specializations in the pyramidal cell phenotype are an important determinant of species-specific executive cortical functions in primates.

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Section: Discussionmentioning

confidence: 99%

Pyramidal cells in prefrontal cortex of primates: marked differences in neuronal structure among species

Elston¹,

Benavides-Piccione

Elston³

et al. 2011

Front. Neuroanat.

105

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“…1992; Van Brederode & Snyder, 1992; Arimatsu et al. 1994; Einstein, 1 996; Matsubara et al. 1996; Zhong‐Wei & Deschenes, 1 997; Prieto & Winer, 1 999; Qi et al.…”

Section: Spiny Inverted Neuronsmentioning

confidence: 99%

The underside of the cerebral cortex: layer V/VI spiny inverted neurons

2007

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This paper presents an account of past and current research on spiny inverted neurons -alternatively also known as 'inverted pyramidal neurons' -in rats, rabbits and cats. In our laboratory, we have studied these cells with a battery of techniques suited for light and electron microscopy, including Nissl staining, Golgi impregnation, dye intracellular filling and axon retrograde track-tracing. Our results show that spiny inverted neurons make up less than 8.5 and 5.5% of all cortical neurons in the primary and secondary rabbit visual cortex, respectively. Infragranular spiny inverted neurons constitute 15 and 8.5% of infragranular neurons in the same animal and areas. Spiny inverted neurons congregate at layers V-VI in all studied species. Studies have also revealed that spiny inverted neurons are excitatory neurons which furnish axons for various cortico-cortical, cortico-claustral and cortico-striatal projections, but not for non-telencephalic centres such as the lateral and medial geniculate nuclei, the colliculi or the pons. As a group, each subset of inverted cells contributing to a given projection is located below the pyramidal neurons whose axons furnish the same centre. Spiny inverted neurons are particularly conspicuous as a source of the backward cortico-cortical projection to primary visual cortex and from this to the claustrum. Indeed, they constitute up to 82% of the infragranular cells that furnish these projections. Spiny inverted neurons may be classified into three subtypes according to the point of origin of the axon on the cell: the somatic basal pole which faces the cortical outer surface, the somatic flank and the reverse apical dendrite. As seen with electron microscopy, the axon initial segments of these subtypes are distinct from one another, not only in length and thickness, but also in the number of received synaptic boutons. All of these anatomical features together may support a synaptic-input integration which is peculiar to spiny inverted neurons. In this way, two differently qualified streams of axonal output may coexist in a projection which arises from a particular infragranular point within a given cortical area; one stream would be furnished by the typical pyramidal neurons, whereas spiny inverted neurons would constitute the other source of distinct information flow.

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“…In the upper layers of visual cortex of both cats and monkeys, there is a relationship between the soma size of pyramidal cells and their connectivity. In cat, pyramidal neurons in layers 2 and 3 projecting locally within area V2 have a mean somatic area only 61% as large as neurons sending axons through the corpus callosum to the contralateral hemisphere (Matsubara et al 1996). Similarly, in macaque monkeys pyramidal neurons in layer 3B of area V1 with only local connections have smaller somata than pyramidal cells that project out of V1 into the white matter (E. M. Callaway, personal communication).…”

Section: Connectivity and Neuron Sizementioning

confidence: 99%

Physiological Properties of Macaque V1 Neurons are Correlated With Extracellular Spike Amplitude, Duration, and Polarity

Gur

Beylin

Snodderly

1999

Journal of Neurophysiology

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In the lateral geniculate nucleus (LGN) the large neurons of the magnocellular layers are functionally distinct and anatomically segregated from the small neurons of the parvocellular layers. This segregation of large and small cells is not maintained in the primary visual cortex (V1); instead a heterogeneous mixture of cells occurs, particularly in the output layers. Nevertheless, our results indicate that for the middle and upper layers of V1, cell size remains a predictor of physiological properties. We recorded extracellularly from neurons in V1 of alert monkeys and analyzed the amplitude, duration, and polarity of the action potentials of 199 cells. Of 156 cells that could be assigned to specific cortical layers, 137 (88%) were localized to the middle and upper cortical layers, layer 4 and above. We summarize evidence that the large-amplitude spikes are discharged by large cells, whereas small-amplitude spikes are the action potentials of smaller cells. Large spikes were predominantly negative and of longer duration, whereas small spikes were predominantly positive and briefer. The putative large cells had lower ongoing activity, smaller receptive field activating regions and higher selectivity for stimulus geometry and stimulus motion than the small cells. The contrasting properties of the large and the small cells were illustrated dramatically in simultaneous recordings made from adjacent cells. Our results imply that there may be an anatomic pairing or clustering of small and large cells that could be integral to the functional organization of the cortex. We suggest that the small and the large cells of area V1 have different roles, such that the small cells may shape the properties of the large output cells. If some of the small cells are also output cells, then cell size should be a predictor of the type of information being sent to other brain regions. Because of their high activity and relative ease of stimulation, the small cells also may contribute disproportionately to in vivo images based on metabolic responses such as changes in blood flow.

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Comparative morphology of three types of projection‐identified pyramidal neurons in the superficial layers of cat visual cortex

Cited by 11 publications

References 0 publications

Pyramidal cells in prefrontal cortex of primates: marked differences in neuronal structure among species

Pyramidal cells in prefrontal cortex of primates: marked differences in neuronal structure among species

The underside of the cerebral cortex: layer V/VI spiny inverted neurons

Physiological Properties of Macaque V1 Neurons are Correlated With Extracellular Spike Amplitude, Duration, and Polarity

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