Connections of the marmoset rostrotemporal auditory area: express pathways for analysis of affective content in hearing

Abstract

The current hierarchical model of primate auditory cortical processing proposes a core of 'primary-like' areas, which is surrounded by secondary (belt) and tertiary (parabelt) regions. The rostrotemporal auditory cortical area (RT) remains the least well characterized of the three proposed core areas, and its functional organization has only recently come under scrutiny. Here we used injections of anterograde and retrograde tracers in the common marmoset (Callithrix jacchus) to examine the connectivity of RT and its adjacent areas. As expected from the current model, RT exhibited dense core-like reciprocal connectivity with the ventral division of the medial geniculate body, the rostral core area and the auditory belt, but had weaker connections with the parabelt. However, RT also projected to the ipsilateral rostromedial prefrontal cortex (area 10), the dorsal temporal pole and the ventral caudate nucleus, as well as bilaterally to the lateral nucleus of the amygdala. Thus, RT has connectivity with limbic structures previously believed to connect only with higher-order auditory association cortices, and is probably functionally distinct from the other core areas. While this view is consistent with a proposed role of RT in temporal integration, our results also indicate that RT could provide an anatomical 'shortcut' for processing affective content in auditory information.

Claustrum projections to prefrontal cortex in the capuchin monkey (Cebus apella)

“…Auditory connections are somewhat more difficult to characterize. We have observed sparse auditory cortex connections in the marmoset (Reser et al, 2009), and other groups have reported claustrum projections to auditory areas in the macaque (Smiley et al, 2007). Where topographic information has been provided, auditory connections were restricted to the ventral claustrum (Pearson et al, 1982).…”

“…Previous tracing studies of claustral projections in primates have shown localized sensory cortical connections within the body of the claustrum (Reviewed in Druga, 2014; visual cortex- Tigges et al, 1982; Doty, 1983; Baizer et al, 1997; Gattass et al, 2014; somatosensory cortex- Pearson et al, 1982; Minciacchi et al, 1991; auditory cortex- Pearson et al, 1982; Smiley et al, 2007; Reser et al, 2009). As mentioned above, it is currently impossible to draw complete homologies of the claustrum anatomy of primate species, though some general patterns have emerged.…”

Asymmetrical effects of unilateral right or left amygdala damage on auditory cortical processing of vocal emotions

“…Previous studies consistently found differential activity in several subregions of auditory cortex in response to vocal emotions (29,30), as well as in the amygdala (4,5,29,31,32), especially for angry voices (3)(4)(5). These auditory effects predominate in the superior temporal gyrus (STG) and superior temporal sulcus (STS), attributed to the processing of emotional valence in the amygdala (10) and presumably mediated by direct anatomical connections between the latter and auditory cortex (9,33). Previous studies also consistently reported a response to emotional voices in the inferior frontal cortex, which may support higher level categorization processes (34) and thus constitutes an important component of the distributed network involved in detecting and decoding vocal emotions (29,35).…”

The cortical motor system of the marmoset monkey (Callithrix jacchus)

“…At the same time, it is also important to recognize that validation of the proposed homologies, based on anatomical connectivity and functional properties, is still lacking in many cases. Studies of selected areas of the sensory (Krubitzer and Kaas, 1990;Rosa and Tweedale, 2000;e.g., Huffman and Krubitzer, 2001;Qi et al, 2002;Rosa et al, 2005;de la Mothe et al, 2006;Palmer and Rosa, 2006a,b;Iyengar et al, 2007;Reser et al, 2009;Rosa et al, 2009; for a recent review, see Solomon and Rosa, 2014) and prefrontal (Burman et al, 2006(Burman et al, , 2011Roberts et al, 2007;Burman and Rosa, 2009;Reser et al, 2013) cortex have revealed essential similarities between marmosets and other species of monkey used in neuroscience research, and clarified homologies. However, much still needs to be accomplished before we can be in a position to confidently extrapolate results across different species of non-human primate, and humans.…”