Dorsal prefrontal and premotor cortex of the ferret as defined by distinctive patterns of thalamo-cortical projections

Abstract

Recent studies of the neurobiology of the dorsal frontal cortex (FC) of the ferret have illuminated its key role in the attention network, top-down cognitive control of sensory processing, and goal directed behavior. To elucidate the neuroanatomical regions of the dorsal FC, and delineate the boundary between premotor cortex (PMC) and dorsal prefrontal cortex (dPFC), we placed retrograde tracers in adult ferret dorsal FC anterior to primary motor cortex and analyzed thalamo-cortical connectivity. Cyto-and myeloarchitectural differences across dorsal FC and the distinctive projection patterns from thalamic nuclei, especially from the subnuclei of the medial dorsal (MD) nucleus and the ventral thalamic nuclear group, make it possible to clearly differentiate three separate dorsal FC fields anterior to primary motor cortex: polar dPFC (dPFCpol), dPFC, and PMC. Based on the thalamic connectivity, there is a striking similarity of the ferret's dorsal FC fields with other species. This possible homology opens up new questions for future comparative neuroanatomical and functional studies.

The diencephalon of two carnivore species: The feliform banded mongoose and the caniform domestic ferret

“…The MD nucleus was the largest of these three nuclei, occupied approximately two thirds of the rostrocaudal extent of the dorsal thalamus, and the left and right MD nuclei do not fuse across the midline. In both species the MD could be subdivided into dorsal (MDd), magnocellular (MDm), and ventral (MDv) subnuclei, based on variations in neuronal soma sizes (a parcellation in agreement with recent connectional studies, Radtke‐Schuller et al, 2020). In all three subnuclei there was a moderate density of neurons, and within the MDm the average size of the soma was slightly larger than in the MDd and MDv, a finding supported by the immunostaining of neuronal soma and dendrites by neurofilament H in the MDm with no staining in the other subnuclei (Figure 15c,d).…”

“…Several studies have examined aspects of the visual nuclei of the domestic ferret dorsal thalamus, including adult connectivity (Akerman, Tolhurst, Morgan, Baker, & Thompson, 2003; Dell, Innocenti, Hilgetag, & Manger, 2019a; Dell, Innocenti, Hilgetag, & Manger, 2019b; Dell, Innocenti, Hilgetag, & Manger, 2019c; Manger, Masiello, & Innocenti, 2002; Manger, Restrepo, & Innocenti, 2010; Morgan, Henderson, & Thompson, 1987), development (Cucchiaro & Guillery, 1984; Guillery, LaMantia, Robson, & Huang, 1985; Hahm, Cramer, & Sur, 1999; Linden, Guillery, & Cucchiaro, 1981; Restrepo, Manger, & Innocenti, 2002; Speer, Mikula, Huberman, & Chapman, 2010), and the developmental and adult expression of certain molecules (Kawasaki, Crowley, Livesey, & Katz, 2004). The somatosensory (Vázquez‐García, Wallman, & Timofeev, 2014), motor (Radtke‐Schuller et al, 2020), auditory (Angelucci, Clascá, Bricolo, Cramer, & Sur, 1997; Angelucci, Clascá, & Sur, 1998), and more general physiological portions of the domestic ferret dorsal thalamus (Monckton & McCormick, 2002) have also been investigated. In addition, studies of the domestic ferret ventral thalamus (Mitrofanis, 1994a, 1994b) and epithalamus (David & Herbert, 1973; David, Herbert, & Wright, 1973; Herbert, 1969, 1971, 1972; Johnson, Meyer, Westaby, & Herbert, 1974; Trueman & Herbert, 1970) are available.…”

Decreased grey matter volume in dorsolateral prefrontal cortex and thalamus accompanied by compensatory increases in middle cingulate gyrus of premature ejaculation patients

“…Cognitive control of behavior is supported by a top-down circuit composed of both the prefrontal cortex and subcortical structures including thalamus. [46][47][48] The thalamus is found to be a key mediator in the thalamo-cortical circuits, which involve in the top-down control of rewarding stimulus-motivated behavior via information updating. 49,50 The thalamus is also considered as the input modulator of the brain, where external sensory stimuli enter the brain, and then sensory information is transmitted to the cortex, especially prefrontal cortex for higher-level processing.…”

The Ferret as a Model System for Neocortex Development and Evolution

“…Ferret frontal cortex lies in the anterior sigmoid, posterior sigmoid, proreal and the orbital gyri at the most rostral part of the brain ( Duque and McCormick, 2010 ; Fritz et al, 2010 ; Radtke-Schuller et al, 2020 ; Figure 2C ). Contrary to primate frontal lobe, in the ferret there is no recognizable anatomical boundary on the cortical surface that can delimit motor areas from the rest of the frontal cortex.…”

“…Furthermore, the ferret lacks a clear granular layer, which is used in primates to define the prefrontal cortex. However, the primary motor cortex has been identified in ferret thanks to the large pyramidal cells in layer V that characterize this area ( Radtke-Schuller et al, 2020 ; Figure 2C ). The connectivity and neuroanatomy of the ferret frontal cortex has been increasingly of interest to the scientific community for studies regarding cognitive control of sensory processing and attention as well as goal-directed behavior ( Fritz et al, 2010 ; Sellers et al, 2016 ; Zhou et al, 2016b ).…”