Architectonic characteristics of the visual thalamus and superior colliculus in titi monkeys

Abstract

Titi monkeys are arboreal, diurnal New World monkeys whose ancestors were the first surviving branch of the New World radiation. In the current study, we use cytoarchitectonic and immunohistochemical characteristics to compare titi monkey subcortical structures associated with visual processing with those of other well-studied primates. Our goal was to appreciate features that are similar across all New World monkeys, and primates in general, versus those features that are unique to titi monkeys and other primate taxa. We examined tissue stained for Nissl substance, cytochrome oxidase (CO), acetylcholinesterase (AChE), calbindin (Cb), parvalbumin (Pv), and vesicular glutamate transporter 2 (VGLUT2) to characterize the superior colliculus, lateral geniculate nucleus, and visual pulvinar. This is the first study to characterize VGLUT2 in multiple subcortical structures of any New World monkey. Our results from tissue processed for VGLUT2, in combination with other histological stains, revealed distinct features of subcortical structures that are similar to other primates, but also some features that are slightly modified compared to other New World monkeys and other primates. These included subdivisions of the inferior pulvinar, sublamina within the stratum griseum superficiale (SGS) of the superior colliculus, and specific koniocellular layers within the lateral geniculate nucleus. Compared to other New World primates, many features of the subcortical structures that we examined in titi monkeys were most similar to those in owl monkeys and marmosets, with the lateral geniculate nucleus consisting of two main parvocellular layers and two magnocellular layers separated by interlaminar zones or koniocellular layers.

Neuronal density and expression of calcium‐binding proteins across the layers of the superior colliculus in the common marmoset (Callithrix jacchus)

“…The density of CB-expressing neurons followed a steep gradient from the superficial to deep layers of the SC, leading to a decrease in the proportion of CB-expressing neurons in the same direction. This observation in the marmoset SC agrees with most studies in primates, including those in the SC of Cebus, titi, and macaque monkeys (Baldwin & Krubitzer, 2018;Glezer et al, 1998;McHaffie et al, 2001;Mize & Luo, 1992;Soares et al, 2001). Indeed, the three-tiered arrangement for CB, described by McHaffie et al (2001) in macaque monkeys, can also be observed in marmoset SC.…”

“…However, studies in primates so far have been based solely on qualitative assessments. In New World titi monkeys, it has been described that the occurrence of CBand PV-stained neurons decreases gradually from dorsal to ventral layers of the SC (Baldwin & Krubitzer, 2018), whereas observations in…”

“…are among the known markers present in some populations of SC neurons (Baldwin & Krubitzer, 2018;Bischop et al, 2012;Kook et al, 2014;McHaffie et al, 2001;Soares et al, 2001). However, studies in primates so far have been based solely on qualitative assessments.…”

The Evolution of the Pulvinar Complex in Primates and Its Role in the Dorsal and Ventral Streams of Cortical Processing

“…In agreement, the receptive fields of neurons in these nuclei reflect those of neurons in V1 and not those of neurons in the superior colliculus [56,57]. While in primates, the superior colliculus does project to both PIcl and PL, the projections are relatively sparse and species variable [52] and they express little or no VGLUT2 in their terminals [33][34][35]51]. These inputs from the superior colliculus may have a suppressive effect on visual excitability of pulvinar neurons during eye movements [58].…”

“…The cells within the superior colliculus that project to PIp and PIcm contain vesicular glutamate transporter 2 mRNA [14,33]. The terminals of these cells express VGLUT2 protein within the pulvinar resulting in PIp and PIcm staining darkly for VGLUT2 protein (grey: [14,33,51], The superior colliculus does not project to the medial division of the inferior pulvinar (PIm: [40,41,52], but PIm is this division that has strong connections with MT (see blue arrows). The image of the superior colliculus shows a coronal view of the dorsal layers of the superior colliculus: The stratum zonale (SZ), the upper stratum griseum superficiale (uSGS), the lower griseum superficiale (lSGS), the stratum opticum (SO), and the stratum griseum intermediate (SGI).…”