Cortico-cortical connections of areas 44 and 45B in the macaque monkey
Introduction
In the human brain, cytoarchitectonic areas 44 and 45 make up Broca’s region (Amunts et al., 1999) which is thought to be critical for certain aspects of language production (Geschwind, 1970, Grodzinsky and Amunts, 2006). Although the homologues of Broca’s region, areas 44 and 45, in the macaque monkey have been established by comparative architectonic studies and electrophysiological recording (Petrides et al., 2005, Petrides and Pandya, 1994, Petrides and Pandya, 2002a, Petrides and Pandya, 2009) and their connections from the inferior parietal lobule and the superior temporal region have been examined (Petrides & Pandya, 2009), several aspects of their cortico-cortical connectivity require clarification. In the monkey brain, area 44 is buried deep in the fundus of the inferior ramus of the arcuate sulcus and is bounded, anteriorly, by area 45B and, posteriorly, by area 6VR (Fig. 1). Dorsally areas 44 and 45B are replaced by area 8Av. Anteriorly, area 45B is replaced by area 45A which continues on the ventrolateral frontal cortex as far as the infraprincipal dimple (Fig. 2). The agranular premotor area 6VR adjoins, caudally, dysgranular area 44 in which the granular layer IV begins to emerge. By contrast, area 45 is typical prefrontal granular cortex in which layer IV is well developed (Petrides and Pandya, 1994, Petrides and Pandya, 2002a, Petrides et al., 2005).
Petrides and Pandya, 1984, Petrides and Pandya, 2009, using the autoradiographic method, demonstrated that distinct axonal connections originating in the inferior parietal lobule terminate in the ventrolateral frontal region of the macaque monkey and the projections to the homologues of areas 44, 45B and 45A have been shown to course via branches II and III of the superior longitudinal fasciculus (SLF II, SLF III). Axons originating from the mid-lateral part of the superior temporal gyrus and the adjacent superior temporal sulcus course as part of the extreme capsule to terminate in the ventrolateral frontal region and these form the temporo-frontal extreme capsule fasciculus (TFECF) (Petrides and Pandya, 1988, Petrides and Pandya, 2009). Fibers originating from the caudal part of the supero-lateral temporal lobe form the arcuate fasciculus (Petrides & Pandya, 2009). Data consistent with these findings were also demonstrated in the human brain using diffusion weighted magnetic resonance imaging (Frey, Campbell, Pike, & Petrides, 2008) and, more recently, with resting state connectivity (Kelly et al., 2010).
The present investigation aimed to refine further our understanding of the cortico-cortical connections of areas 44 and 45B of the macaque monkey by injecting retrograde fluorescent tracers in these areas in order to establish the entire set of neurons that send axons to terminate in these two areas. Additional injections into the anterior part of the inferior parietal lobule and the mid-temporal region of the superior temporal gyrus were used to examine further the bi-directionality of connections of the ventrolateral frontal region with these posterior regions of the cortex.
Section snippets
Subjects
The subjects were seven adult macaque monkeys (1 female and 5 male Macaca fascicularis and 1 male Macaca mulatta), 3.7–10 kg (average 6.2 kg) at the time of surgery. The study was approved by the Montreal Neurological Institute Animal Ethics Committee and conformed to the Canadian Council of Animal Care guidelines for humane care of laboratory animals.
Anesthesia and surgery
All surgical procedures were performed under strict aseptic conditions. Fifteen minutes prior to anesthesia, the animal was administered an initial
Case 1 (area 44)
In this case, an injection of Fast Blue was placed in area 44 in the fundus of the inferior ramus of the arcuate sulcus in the left ventrolateral frontal cortex. There was a slight encroachment of the tracer upon area 6VR in the caudal bank of the inferior ramus of the arcuate sulcus (Fig. 3, Fig. 4). Labeled neurons were observed in the adjacent cortical areas 45B, 6VR, proM, and 8Av. Labeled neurons were also observed in area 9/46v which occupies the ventral lip of the principal sulcus and
Discussion
The present experimental anatomical tracer study offers new insights into the corticocortical connectivity of areas 44 and 45B in the macaque monkey by emphasizing the distribution of retrogradely labeled cells that send axons to these specific areas of the ventrolateral frontal cortex. Because these architectonic areas have been delineated using the same criteria in both the monkey and the human brain (Petrides and Pandya, 1994, Petrides and Pandya, 2002a), it is likely that the connectivity
Acknowledgments
This work was supported by the Natural Sciences and Engineering Research Council of Canada (RGPIN 170426-07). We thank Jennifer Novek and Veronika Zlatkina for processing the anatomical tissue, Emily Rubin-Ferreira for preparing the anatomical reconstructions. Jennifer Novek and Callah Boomhaur prepared some of the illustrations.
List of Abbreviations
- AF
- arcuate fasciculus
- AIP
- anterior intraparietal area
- as
- arcuate sulcus
- asd
- anterior subcentral dimple
- cal
- calcarine sulcus
- ciM
- cingulate motor region
- cings
- cingulate sulcus
- cc
- corpus callosum
- cs
- central sulcus
- DI
- dysgranular insula
- DP
- dorsal prelunate area
- ECF
- temporo-frontal extreme capsule fasciculus
- ER
- entorhinal cortex
- FST
- fundus of superior temporal sulcus
- G
- gustatory cortex
- GI
- granular insula
- IPa
- associated area of the superior temporal sulcus
- IPd
- inferior parietal, dorsal part
- iar
- inferior ramus of the arcuate sulcus
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2022, Neuroscience and Biobehavioral ReviewsCitation Excerpt :A second conception comes from researchers who have reconstructed the longitudinal pathways with dMRI tractography based on anatomical priors from macaque tract-tracing experiments (Fig. 3 right panel) (e.g., Barbeau et al., 2020; Frey et al., 2008; Makris et al., 2009; Warrington et al., 2020). Considering that neural tract-tracing is the gold standard for determining the precise origins and terminations, and axonal courses of brain connections, the macaque model that separates the peri-sylvian longitudinal fibres into the AF, SLF I, II and III bundles (i.e., Frey et al., 2014) would constitute the most anatomically accurate model of the primate longitudinal fibre system at present (Fig. 3 right panel). Critically, it remains questionable how generalizable this macaque model is to the human brain, since after all language (which is associated with the AF) is not present in the macaque.