Corticocortical interactions between and within three cortical auditory areas specialized for time-domain signal processing

Abstract

In auditory cortex of the mustached bat, the FF (F means frequency modulation), dorsal fringe (DF), and ventral fringe (VF) areas consist of "combination-sensitive" neurons tuned to the pair of an emitted biosonar pulse and its echo with a specific delay (best delay: BD). The DF and VF areas are hierarchically at a higher level than the FF area. Focal electric stimulation of the FF area evokes "centrifugal" BD shifts of DF neurons, i.e., shifts away from the BD of the stimulated FF neurons, whereas stimulation of the DF neurons evokes "centripetal" BD shifts of FF neurons, i.e., shifts toward the BD of the stimulated DF neurons. In our current studies, we found that the feedforward projection from FF neurons evokes centrifugal BD shifts of VF neurons, that the feedback projection from VF neurons evokes centripetal BD shifts of FF neurons, that the contralateral projection from DF neurons evokes centripetal BD shifts of DF neurons, and that the centripetal BD shifts evoked by the DF and VF neurons are 2.5 times larger than the centrifugal BD shifts evoked by the FF neurons. The centrifugal BD shifts shape the selective neural representation of a specific target distance, whereas the centripetal BD shifts expand the representation of the selected specific target distance to focus on the processing of the target information at a specific distance. The centrifugal and centripetal BD shifts evoked by the feedforward and feedback projections promote finer analysis of a target at shorter distances.

Figure 1.

The auditory cortex, the delay-tuned areas, and the responses of a delay-tuned neuron. A, Dorsolateral view of the left cerebral cortex of the mustached bat. “1–7” are respectively the DSCF, Ala (anterior division of AI), Alp (posterior division of AI), FF, CF/CF, DF, and VF areas. The FF area was previously called the FM–FM area. B, The FF, DF, and VF areas each consist of three types of combination-sensitive neurons called FM₁–FM₂, FM₁–FM₃, and FM₁–FM₄ delay-tuned neurons. The subscripts 1–4 indicate the first through fourth harmonics of FM components of biosonar pulses and echoes. C, The array of PST histograms displaying the responses of a VF neuron to pulse FM₁ alone (P), echo FM₂ alone (E), and P–E pairs with different echo (E) delays ranging from 0.0 to 9.5 ms. The best delay for the facilitatory response of the neuron was 1.0 ms.

Figure 2.

Changes in the responses and delay–response curves of a single VF neuron and a VF evoked potential evoked by electric stimulation of BD-unmatched FF neurons. A1, The recorded VF neuron was tuned to a FM₁–FM₂ with a 3.0 ms delay, whereas the stimulated FF neurons were tuned to a FM₁–FM₂ with a 7.0 ms delay. The arrays of PST histograms display the responses of the VF neuron at its BDs in the control (BD_c) and shifted (BD_s) conditions to paired FM₁–FM₂ stimuli obtained before, 85 min after, and 137 min after the onset of the FF electric stimulation. A2, The delay–response curves of the VF neuron obtained before (open circles, control), 85 min after (filled circles), and 137 min after (open triangles, dashed line) the onset of the FF stimulation. B1, The VF evoked potential was tuned to a FM₁–FM₂ with a 4.5 ms delay, whereas the stimulated FF neurons were tuned to a FM₁–FM₂ with a 7.0 ms delay. The evoked potentials at their BD_c and BD_s elicited by paired FM₁–FM₂ sounds were recorded before, 77 min after, and 137 min after the onset of the FF stimulation. B2, The delay–response curves of the VF evoked potential obtained before (open circles, control), 77 min after (filled circles), and 137 min after (open triangles, dashed line) the onset of the FF stimulation.

Figure 3.

BD shifts as a function of the BD difference between the recorded and stimulated neurons. A, The BD shifts of 16 VF neurons (open circles) and five evoked potentials (filled circles) evoked by electric stimulation of FF neurons. FF-to-VF, A feedforward projection from the FF area to the VF area. B, The BD shifts of 18 FF neurons (triangles) evoked by electric stimulation of VF neurons. VF-to-FF, A feedback projection from the VF area to the FF area. C, The BD shifts of one contralateral DF neuron (open square) and six contralateral DF evoked potentials (filled squares) evoked by electric stimulation of DF neurons. DF-to-cDF, Projection from the DF area to the contralateral DF area.

Figure 4.

Changes in the responses and delay–response curves of a single BD-unmatched (A) and a single BD-matched (B) FF neuron evoked by electric stimulation of VF neurons. The recorded FF and stimulated VF neurons both were tuned to a combination of FM₁ and FM₂. A, The best delays of the recorded FF and stimulated VF neurons were 3.5 and 2.0 ms, respectively. B, The BDs of the recorded and stimulated neurons both were 1.5 ms. See Figure 2 legend for abbreviations and symbols.

Figure 5.

Changes in the responses and delay–response curves of a single DF neuron (A) and a DF evoked potential (B) evoked by electric stimulation of contralateral BD-unmatched DF neurons. A, The DF neuron was tuned to a FM₁–FM₂ with a 4.0 ms delay, and the stimulated contralateral DF neurons were tuned to FM₁–FM₂ with a 2.0 ms delay. B, The DF evoked potential was tuned to a FM₁–FM₂ with a 5.0 ms delay, and the stimulated contralateral DF neurons were tuned to a FM₁–FM₂ with a 3.0 ms delay. See Figure 2 legend for abbreviations and symbols.

Figure 6.

The BD shift-difference curves for the BD shifts evoked by electric stimulation of either the FF (A), DF (B), or VF (C) neurons and the block diagram showing feedforward, feedback, lateral, and contralateral modulations (D). A, “1–5” respectively show the curves for the BD shifts elicited by the lateral, contralateral feedforward to DF or VF and corticofugal projections from (or within) the FF area. B, “1–3” respectively show the curves for the BD shifts elicited by the feedback, lateral, and contralateral projections from (or within) the DF area. C, “1” shows the curve for the BD shifts elicited by the feedback projection to the FF area from the VF area. D, The block diagram showing the projections evoking the centripetal and centrifugal BD shifts. The projections evoking the centripetal BD shifts are indicated by the arrows, whereas those evoking the centrifugal BD shifts are indicated by the lines with a short bar at the end. The dotted lines indicate either centripetal or centrifugal BD shifts which are speculated to be evoked. This summary figure is based on the data obtained by Yan and Suga (1996), Xiao and Suga (2004), Tang et al. (2007), Tang and Suga (2008), and our current studies.