Development of parallel auditory thalamocortical pathways for two different behaviors

Abstract

Auditory thalamocortical connections are organized as parallel pathways that originate in different divisions of the medial geniculate body (MGB). These pathways may be involved in different functions. Surprisingly little is known about the development of these connections. Here we review studies of the organization and development of auditory thalamocortical pathways in the pallid bat. The pallid bat depends primarily on passive hearing of prey-generated noise for localizing prey, while reserving echolocation for general orientation and obstacle avoidance. In the inferior colliculus (IC) and the auditory cortex, physiological studies show that noise and echolocation calls are processed in segregated regions. Injection of retrograde tracers in physiologically characterized cortical sites show that the ventral division of the MGB (MGBv) projects to the cortical region selective for noise. The cortical region selective for echolocation calls receives input from the suprageniculate (SG) nucleus in the dorsal MGB, but not from the MGBv. Taken together, these studies reveal parallel IC-MGB-cortex pathways involved in echolocation and passive listening. There is overlap of thalamocortical pathways during development. At 2-weeks postnatal, when the bat begins to exhibit adult-like hearing thresholds, the SG projects to both noise- and echolocation call-selective regions. The MGBv, as in adults, projects only to the noise-selective region. The connections become adult-like only after 2-months postnatal. These data suggest that parallel auditory thalamocortical pathways may segregate in an experience-dependent fashion, a hypothesis that remains to be tested in any species.

Keywords: auditory cortex; auditory development; echolocation; medial geniculate body; parallel pathways; plasticity; thalamocortical.

Figure 1

Schematic of thalamocortical pathways in adult mustached, horseshoe and pallid bats and young pallid bat. (A) In the horseshoe bat, the MGBd projects mainly to regions dorsal to A1 that contain the combination-sensitive neurons used in target distance computation. The MGBv projects to A1. In the mustached bat, the rostral pole nucleus projects to the delay-tuned areas. It is not clear if the rostral pole nucleus should be considered a part of the ventral or dorsal MGB. Therefore, the term “MGBd/MGBv-RP” is used in this schematic. In both species, the SG, considered a part of the MGBd, projects diffusely but more to the non-primary cortex than primary cortex. (B) In adult pallid bats, the HFR involved in echolocation behavior receives input from the SG and the MGBd, but not the MGBv. The LFR, involved in passive localization, receives input from the MGBv, but not the SG. Based on response selectivity in the auditory cortex, the SG → HFR pathway is involved in echolocation behavior while the MGBv → LFR pathway is involved in passive localization of prey-generated noise. (C) In a 2-week-old pallid bat pup, however, the pathways overlap. This is because the SG projects to both the LFR and HFR. The pup MGBv, as in adults, does not project to the HFR. Thus anatomically segregated pathways arise through postnatal refinement of initially overlapping connections.

Figure 2

Parallel thalamocortical pathways in the adult pallid bat auditory system. I (A–F) An example of injection made in the HFR. (A) Fluorogold (FG) injection site. (B) Frequency selectivity of injection site. The injection was made near neurons tuned ∼42 kHz and selective for downward FM sweeps. (C–F) Photomicrographs of increasingly more rostral locations of the MGB show that labeled neurons were found in the SG, MGBm, and MGGd, but not in the MGBv. II (G–P) An example of injections made in the LFR. (G) FG injection site (H) Fluororuby (FR) injection site. (I) FG was injected near neurons tuned ∼26 kHz. FR was injected near neurons tuned ∼15 kHz. (J–N) Schematics of increasingly rostral sections through the MGB showing that labeled neurons were found in the MGBv, MGBm, and MGBd, but not the SG. (O,P) Photomicrographs showing FG and FR labeled cells near the rostrocaudal center of the MGB. III (Q–S) An experiment in which FG was injected in the LFR and FR was injected in the HFR. (Q) Schematic of injection sites. (R) Schematic of a section at the rostrocaudal center of the MGB showing that FG labeled neurons were present in MGBv, but not the SG, and that FR labeled cells were found in the SG, but not the MGBv. (S) Photomicrograph of the section shown in (R).

Figure 3

The thalamocortical pathways overlap during early development. This occurs because the SG projects to both LFR and HFR in pups. I (A–J) LFR injection in a P15 pup. (A) FG was injected in the LFR near sites with tuning ∼15 kHz. (B) FG injection site. (C–F) Photomicrographs of increasingly rostral sections through the MGB demonstrate that both the SG and MGBv show labeled cells. (G,H) Magnified view of the SG and (I,J) MGBv show strong label in both areas. It can also be noted that caudal SG sends more projections to the LFR in pups than rostral SG. II (K–S) HFR injection in a P20 pup. (K) The injection site had best frequencies near 40 kHz. (L) FG injection site. (M–P) Schematic and (Q–S) Photomicrographs of the MGB show that labeled cells were present in the SG and MGBd, but not the MGBv. III (T–Z) Injections in both LFR and HFR. (T) FG was injected in the LFR. FR was injected in the HFR. (U) Injection sites. (V–Y) FG and FR labeled cells were seen in the SG, while only FG labeled cells were seen in the MGBv. (Z) Magnified view of the SG shows FG and FR labeled cells, although no double labeled cells were seen. Scale bars: 500 μm in B–F; 200 μm in G–J.