Feedforward and feedback projections of caudal belt and parabelt areas of auditory cortex: refining the hierarchical model

Abstract

Our working model of the primate auditory cortex recognizes three major regions (core, belt, parabelt), subdivided into thirteen areas. The connections between areas are topographically ordered in a manner consistent with information flow along two major anatomical axes: core-belt-parabelt and caudal-rostral. Remarkably, most of the connections supporting this model were revealed using retrograde tracing techniques. Little is known about laminar circuitry, as anterograde tracing of axon terminations has rarely been used. The purpose of the present study was to examine the laminar projections of three areas of auditory cortex, pursuant to analysis of all areas. The selected areas were: middle lateral belt (ML); caudomedial belt (CM); and caudal parabelt (CPB). Injections of anterograde tracers yielded data consistent with major features of our model, and also new findings that compel modifications. Results supporting the model were: (1) feedforward projection from ML and CM terminated in CPB; (2) feedforward projections from ML and CPB terminated in rostral areas of the belt and parabelt; and (3) feedback projections typified inputs to the core region from belt and parabelt. At odds with the model was the convergence of feedforward inputs into rostral medial belt from ML and CPB. This was unexpected since CPB is at a higher stage of the processing hierarchy, with mainly feedback projections to all other belt areas. Lastly, extending the model, feedforward projections from CM, ML, and CPB overlapped in the temporal parietal occipital area (TPO) in the superior temporal sulcus, indicating significant auditory influence on sensory processing in this region. The combined results refine our working model and highlight the need to complete studies of the laminar inputs to all areas of auditory cortex. Their documentation is essential for developing informed hypotheses about the neurophysiological influences of inputs to each layer and area.

Differential maturation of vesicular glutamate and GABA transporter expression in the mouse auditory forebrain during the first weeks of hearing

“…These assays were performed in parallel in adult mouse and macaque monkey tissue, in support of the present study of mice and prior studies of monkeys (Balaram et al 2011; Hackett and de la Mothe 2009; Hackett et al 2014). Antibody specificity was tested by incubating each antibody with a 10× concentration of the control protein provided by the manufacturer, when available.…”

“…NeuN (Fox-3) is one of many members of the RNA-binding protein family (Darnell 2013). Although these proteins are mainly involved in the regulation of mRNA, Fox-3/NeuN is widely used as a neuron-specific marker in adult and developing brain across species (Arellano et al 2012; Fuentes-Santamaria et al 2013; Hackett et al 2014; Kim et al 2009). Antibodies for NeuN produce strong somatic labeling of neurons in most brain areas.…”

Functional organization of human auditory cortex: Investigation of response latencies through direct recordings

“…According to this classic model, primary auditory cortex (AI) and adjacent cortex (areas R and RT) form the core region, surrounded by belt, and then parabelt regions. Neuroanatomical tracing studies demonstrate that each area has strong bidirectional connectivity with adjacent areas such that core areas are directly interconnected with their neighboring belt, but have sparse interconnections with parabelt areas (for review, see Jones, 2003; Hackett et al, 2014). More complex connectivity patterns are currently being characterized that refine this simplified scheme, including feedforward projections from parabelt to belt (Hackett et al, 2014).…”

“…Neuroanatomical tracing studies demonstrate that each area has strong bidirectional connectivity with adjacent areas such that core areas are directly interconnected with their neighboring belt, but have sparse interconnections with parabelt areas (for review, see Jones, 2003; Hackett et al, 2014). More complex connectivity patterns are currently being characterized that refine this simplified scheme, including feedforward projections from parabelt to belt (Hackett et al, 2014). Further confounding the classic serial core-belt-parabelt model of auditory cortical connectivity are the complex parallel pathways emanating from the medial geniculate complex (Jones, 2003).…”

Anatomic organization of the auditory cortex

“…HACKETT temporal area), the insula, and poorly defined areas of the circular sulcus, such as Pro, part of which extends to the temporal pole. However, there is also substantial overlap of rostral and caudal areas of the belt and parabelt along this axis, and the connections with other cortical and sensory regions can be patchy, overlapping, or interdigitating Pandya, 1978, 1994;Galaburda and Pandya, 1983;Cipolloni and Pandya, 1985;Barnes and Pandya, 1992;Cusick et al, 1995;Seltzer et al, 1996;Hackett et al, 1998aHackett et al, , 2014. Laterally, the principal connections of the auditory (belt, parabelt) and auditory-related areas of the STG are with areas in the fundus and upper bank of the STS, known as the superior temporal polysensory region (STP).…”