Auditory connections and functions of prefrontal cortex

Abstract

The functional auditory system extends from the ears to the frontal lobes with successively more complex functions occurring as one ascends the hierarchy of the nervous system. Several areas of the frontal lobe receive afferents from both early and late auditory processing regions within the temporal lobe. Afferents from the early part of the cortical auditory system, the auditory belt cortex, which are presumed to carry information regarding auditory features of sounds, project to only a few prefrontal regions and are most dense in the ventrolateral prefrontal cortex (VLPFC). In contrast, projections from the parabelt and the rostral superior temporal gyrus (STG) most likely convey more complex information and target a larger, widespread region of the prefrontal cortex. Neuronal responses reflect these anatomical projections as some prefrontal neurons exhibit responses to features in acoustic stimuli, while other neurons display task-related responses. For example, recording studies in non-human primates indicate that VLPFC is responsive to complex sounds including vocalizations and that VLPFC neurons in area 12/47 respond to sounds with similar acoustic morphology. In contrast, neuronal responses during auditory working memory involve a wider region of the prefrontal cortex. In humans, the frontal lobe is involved in auditory detection, discrimination, and working memory. Past research suggests that dorsal and ventral subregions of the prefrontal cortex process different types of information with dorsal cortex processing spatial/visual information and ventral cortex processing non-spatial/auditory information. While this is apparent in the non-human primate and in some neuroimaging studies, most research in humans indicates that specific task conditions, stimuli or previous experience may bias the recruitment of specific prefrontal regions, suggesting a more flexible role for the frontal lobe during auditory cognition.

Keywords: acoustic; frontal lobe; monkey; working memory.

Figure 1

Top panel are schematics of the lateral and frontal surfaces of the monkey (A) and human (B) brain from Petrides and Pandya (2002). Bottom panel are schematics illustrating area 12 vl (now referred to as 12/47) and 12 orb (C) and a coronal section (D) depicting these regions from Preuss and Goldman-Rakic (1991). Inset diagram is the lower part of arcuate sulcus to show cytoarchitectonic areas within the banks of the sulcus. Used/modified with permission from Petrides and Pandya (2002) and Preuss and Goldman-Rakic (1991).

Figure 2

Connections of VLPFC with auditory cortex. An injection of WGA-HRP shown previously (Romanski et al., 1999a) illustrates the density of connections of VLPFC with auditory cortical regions in the belt, parabelt and superior temporal sulcus as well as the rostral temporal lobe. Coronal sections through the temporal lobe are shown in (A–C) with black dots illustrating the location of retrogradely labeled cells. Labeling is heaviest in the superior temporal sulcus regions TPO and TAa, moderate in the parabelt and lighter in the lateral belt. (D) A photomicrograph from a temporal lobe section adjacent to that shown in (B). (E) Is a photomicrograph of the prefrontal cortex section containing the injection site for this injection which was located in the ventral part of area 12/47. (F) Portrays the location of the injection site in VLPFC and the locations of the coronal sections from A–C on a lateral schematic of the macaque brain. Adapted from Romanski et al. (1999a).

Figure 3

A circuit diagram summary of auditory inputs from temporal lobe areas to the PFC, from anatomical studies (including: Petrides and Pandya, ; Seltzer and Pandya, ; Hackett et al., ; Romanski et al., 1999a,b) discussed in this review. Thicker lines represents stronger connections. R, Rostral; C, Caudal; STS, Superior Temporal Sulcus; STG, Superior Temporal Gyrus; AL, Antero-lateral; ML, Middle-lateral; CL, Caudal-lateral; TPO, temporal parieto-occiptal area; TAa, Temporal area.

Figure 4

Schematic diagram illustrating the flow of information from the auditory cortex to the VLPFC. Thick and dark gray arrows illustrate dense projections from STS, with less dense projections arriving from parabelt and lateral belt regions. AL, Antero-lateral; R, Rostral; STS, Superior Temporal Sulcus; STG, Superior Temporal Gyrus; TPO, temporal parieto-occiptal area; TAa, Temporal area.

Figure 5

Example cells with activity occurring during the presentation of the auditory sample, match/nonmatch and during the decision period of an auditory delayed match-to-sample task. (A) An example cell with increased activity during the auditory cues, wait time and response periods for correct trials. (B) An example cell with increased firing rated during auditory cue and wait time periods for correct trials. Y-axis label is frequency (imp/s); bin = 100 ms; asterisk signifies significant change in firing rate from baseline.

Figure 6

Sagittal and horizontal view of human brain on which activations have been plotted across several fMRI studies involving processing of information during tasks that utilized stimuli that were Non-verbal/Spatial (dark green square), Non-verbal/Non-spatial (light green triangle), Verbal/Spatial (dark blue square), and Verbal/Non-spatial (light blue triangle). fMRI coordinates are plotted in Talairach space. Sagittal (x = +29 mm) and horizontal (z = −4 mm), Talairach images for reference from Talairach and Tournoux (1988). For a list of the studies plotted see (Supplemental Table 1).