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Review
. 2021 Jun;22(3):237-259.
doi: 10.1007/s10162-021-00794-3. Epub 2021 Apr 28.

Development of Auditory Cortex Circuits

Minzi Chang  1 , Patrick O Kanold  2
Affiliations
Review

Development of Auditory Cortex Circuits

Minzi Chang et al. J Assoc Res Otolaryngol. 2021 Jun.

Abstract

The ability to process and perceive sensory stimuli is an essential function for animals. Among the sensory modalities, audition is crucial for communication, pleasure, care for the young, and perceiving threats. The auditory cortex (ACtx) is a key sound processing region that combines ascending signals from the auditory periphery and inputs from other sensory and non-sensory regions. The development of ACtx is a protracted process starting prenatally and requires the complex interplay of molecular programs, spontaneous activity, and sensory experience. Here, we review the development of thalamic and cortical auditory circuits during pre- and early post-natal periods.

Keywords: activity; cortex; development; subplate; thalamus.

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Figures

Fig. 1
Fig. 1
Development in hearing across species. The auditory system can respond to sound (high-threshold) even before the ear canal open. The estimated timing for pre-hearing (no responses were recorded during sound-stimuli), high-threshold hearing, and low-threshold hearing is described for the mouse a, cat b, ferret c, and human d. P: postnatal day. GW, gestational week
Fig. 2
Fig. 2
Development of excitatory and inhibitory neurons during the embryonic period. a Cortical excitatory neurons were generated from the radial glial cells and migrate towards their final location within cortical plate (CP) guided by Cajal-Retzius cells. The first generated neurons are the subplate (SP) neurons, followed by deeper layer neurons and upper layer neurons that sequentially migrate into the CP. Cajal-Retzius cells and some subplate neurons largely disappear over development. b Inhibitory neurons are generated from the ganglionic eminence (GE) starting around embryonic days (E)10 and migrate tangentially to the cortex (left). The presence of inhibitory neurons in the intermediate/ventricular zone and marginal zone can be detected at the lateral region of the murine cortex as early as E12.5 (left). Some of these inhibitory neurons will continue to migrate towards the dorsomedial region of the cortex, however, whether the timing of these neurons invading the cortical plate happens concurrently is unclear (middle). Around P14, the inhibitory neurons evenly distributed within the cortex (right). ACtx, auditory cortex; L, layer; MZ, marginal zone; SVZ/VZ, subventricular zone/ventricular zone; VCtx, visual cortex
Fig. 3
Fig. 3
Transient circuits between subplate neurons and thalamocortical axons in auditory cortex. a The first generated neurons are the subplate neurons (SP, gray). These neurons can be detected as early as E11 in the auditory cortex (ACtx), almost similar timing as the thalamic nuclei that are generated in the medial geniculate body (MGB) around E10. The thalamocortical axons from the thalamus contact subplate neurons in ACtx around E13.5. b Thalamocortical axons from the medial geniculate nucleus (MGN) arrive in the SP of ACtx (red) earlier than those from the lateral geniculate nucleus (LGN) in the SP of visual cortex (VCtx, blue). Around postnatal days (P) 5, the thalamocortical fibers arrived in the VCtx layer (L) 4, earlier than those in ACtx. c SP neurons project to thalamorecipient L4 and L1 as well as to MGB during early postnatal ages. Complexin 3 (Cplx3, green) is expressed in SP neurons and strong puncta immunolabeling can be detected at (i) the thalamus surrounding the ventral division of MGN (MGBv), and in (ii) the L4 and L1. Vesicular glutamate transporter 2 (vGlut2, magenta) labelling thalamocortical fibers and thalamorecipient L4. d A transient circuit is formed between the SP and MGB during the early embryonic period, and the SP neurons were projecting to the future L4 neurons (left). During the development, the TCAs from MGB will penetrate the cortex and move towards the L4 neurons (middle). In the adult, when the connections between MGB and L4 are established, the subplate network diminished (right). During this process, SP might be considered a proto-organizational structure, ensuring that L4 is organized in a tonotopic manner. Pseudo-colored represents different frequencies in the tonotopic map. MGBd, dorsal division of MGN; scale bar for c is 1 mm; scale bar for (i, ii) is 50 µm
Fig. 4
Fig. 4
Schematic figure of connections in primary auditory cortical development. Ages refer to mice. a Projections from the medial geniculate body (MGB) arrive in the subplate layers of primary auditory cortex (A1) during embryonic development. After birth, the thalamocortical axons from both MGBd and MGBv refine and terminate into their appropriate target and some SP neurons start to disappear. b In the first postnatal week, L2/3 neurons (purple) establish intracortical networks with their surrounding neurons. Besides ascending L4 inputs, between P9 and P16, L2/3 neurons also receive extensive inputs from L5/6 neurons. Such connections disappear in adulthood. c During early development, long-range corticocortical connections between primary and secondary areas are established mainly by the lower layer and possibly subplate neurons (left). As the cortex matures, the upper layer neurons form long-range corticocortical connections between primary and secondary cortical areas (middle). As the thalamocortical inputs innervate layer 4 and during maturation of upper layer neurons, the corticocortical connections in the lower layers decrease. MZ, marginal zone; CP, cortical plate
Fig. 5
Fig. 5
The connection among thalamus, primary and secondary auditory areas in cat. a In normal hearing, the primary auditory cortex (A1) received inputs from all three divisions of the medial geniculate body (MGB), as well as from other secondary auditory fields. b In congenital deafness, an increase of ectopic connections can be detected (black arrow), while a decline of intra-areal connectivity is present (dotted red line). c, d Early-onset deafness, defined as when the hearing was eliminated near ear canal opening during the critical period, and late-onset deafness defined as the elimination of auditory stimuli after critical period showed different changes in the connections among the thalamus, A1 and other higher-order of auditory fields. a–d Gray: normal connection; Black arrow: increased connection; Red dotted arrow: decreased connection; Bolder arrow: larger changes compared with other conditions. MGBv, ventral division of MGB; MGBd, dorsal division of MGB; MGBm, medial division of MGB; A2, secondary auditory cortex; AAF, anterior auditory field; PAF, posterior auditory field; DZ, dorsal zone
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