The auditory cortex of the bat Phyllostomus discolor: Localization and organization of basic response properties

Abstract

Background: The mammalian auditory cortex can be subdivided into various fields characterized by neurophysiological and neuroarchitectural properties and by connections with different nuclei of the thalamus. Besides the primary auditory cortex, echolocating bats have cortical fields for the processing of temporal and spectral features of the echolocation pulses. This paper reports on location, neuroarchitecture and basic functional organization of the auditory cortex of the microchiropteran bat Phyllostomus discolor (family: Phyllostomidae).

Results: The auditory cortical area of P. discolor is located at parieto-temporal portions of the neocortex. It covers a rostro-caudal range of about 4800 mum and a medio-lateral distance of about 7000 mum on the flattened cortical surface. The auditory cortices of ten adult P. discolor were electrophysiologically mapped in detail. Responses of 849 units (single neurons and neuronal clusters up to three neurons) to pure tone stimulation were recorded extracellularly. Cortical units were characterized and classified depending on their response properties such as best frequency, auditory threshold, first spike latency, response duration, width and shape of the frequency response area and binaural interactions. Based on neurophysiological and neuroanatomical criteria, the auditory cortex of P. discolor could be subdivided into anterior and posterior ventral fields and anterior and posterior dorsal fields. The representation of response properties within the different auditory cortical fields was analyzed in detail. The two ventral fields were distinguished by their tonotopic organization with opposing frequency gradients. The dorsal cortical fields were not tonotopically organized but contained neurons that were responsive to high frequencies only.

Conclusion: The auditory cortex of P. discolor resembles the auditory cortex of other phyllostomid bats in size and basic functional organization. The tonotopically organized posterior ventral field might represent the primary auditory cortex and the tonotopically organized anterior ventral field seems to be similar to the anterior auditory field of other mammals. As most energy of the echolocation pulse of P. discolor is contained in the high-frequency range, the non-tonotopically organized high-frequency dorsal region seems to be particularly important for echolocation.

Figure 1

Recording sites and subfields in the auditory cortex of Phyllostomus discolor. A) Lateral view of the P. discolor brain. Recording sites of all 849 units are indicated as black dots. Superimposed black outlines are neuroanatomically determined borders. Solid black lines represent reliable borders, whereas stippled black lines represent more variable borders. Rostro-caudal positions of frontal sections shown in Fig. 2 are indicated by the white vertical lines. Colored lines represent equal medio-lateral distances from the midline in 1000 μm steps as shown in the flattened cortical surface projection in 1B. B) Projection of recording sites (black crosses) and neuroanatomical borders (black lines) on an unrolled and flattened cortical surface. Lateral distances on the cortical surface are indicated in 1000 μm steps by corresponding colors as in the side view (1A). The origin used for the flattening process was fixed at 2000 μm lateral from the midline of the brain (upper dark blue line). C) Schematic of the auditory cortical subfields: anterior dorsal field (ADF), posterior dorsal field (PDF), anterior ventral field (AVF) and posterior ventral field (PVF) with dorsal (PVFd), ventral (PVFv) parts and a border zone (bz) reconstructed on the flattened cortical surface. The neuroanatomically determined borders are indicated by black lines.

Figure 2

Frontal sections at two rostro-caudal levels. The frontal sections are shown for position indicated by the vertical lines in Fig. 1A. Top row: sections (40 μm thick) stained for cells (Nissl); middle row: neighboring sections stained for myelin; bottom row: sections stained for zinc at comparable rostro-caudal level from another series. Scalebar: 2000 μm. Abbreviations as in Fig. 1C.

Figure 3

Cut-outs of frontal sections from the centers of the different cortical fields. Field names are given in the zinc-stained section and apply to the two neighboring photographs to the right. Indications of layers in the Nissl-stained sections apply to the neighboring left (zinc-stained) and right (myelin-stained) sections, respectively. White arrowheads in the zinc-stained sections indicate the borders of layer IV. Stars in the cut-out of the zinc-stained section of ADF highlight the two components of layer V. The scale bar of 250 μm applies to all cutouts. Abbreviations as in Fig. 1C.

Figure 4

Distribution of response properties of cortical units and examples of PSTHs for different response types. The frequency distribution of neuronal response properties evoked by pure tone stimulation is shown for: A) Best frequency, B) Response threshold, D) First spike latency, E) Response duration and G) Q_10dB values. Peri-stimulus time histograms (PSTHs) show examples of cortical units with different response types: C) phasic response, F) phasic response with a sustained component and I) tonic response. The binwidth of the histograms is 1 ms. The grey bar represents the acoustic stimulus (20 ms pure tone). Panel H) shows the Q_10dB values as a function of best frequency. The regression line is shown in red.

Figure 5

Examples of the six different FRA types of cortical units. Examples of the different classes of FRA types are shown for: A) monotonically V-shaped, B) non-monotonically V-shaped, C) monotonically double tuned, D) non-monotonically double tuned, E) circumscribed and F) complex FRAs.

Figure 6

Spatial representation of response properties on the flattened cortical surface and statistical comparison between the four cortical fields. Tessellation maps of the spatial representation are shown for: A) Best frequency, C) Q_10dB value, F) Response threshold, G) First spike latency and H) Response duration. The outlines of AC and AC subfields are superimposed (black lines as in Fig 1). Panel B) shows the topographic position of the AC subfields of P. discolor derived from neuroarchitectural characteristics. The arrows indicate BF gradients in the tonotopically organized ventral fields. Statistical analysis of different cortical subfields are shown for: D) Best frequency, E) Q_10dB value, I) Response threshold, J) First spike latency and K) Response duration. Box plots show the median (red line) and the 25th and 75th percentiles. The 'whiskers' indicate the limits of the remaining percentiles. Outliers (Values >1.5 times the interquartile range) are not shown in the figure. The thick black lines above the plots indicate significant differences (Kruskal-Wallis test, p < 0.05). Abbreviations as in Fig. 1C.

Figure 7

Spatial representation of FRA types and binaural response types and distribution in different cortical subfields. Spatial representation A) and distribution in cortical subfields C) of the different FRA types. V/D mon: monotonically V-shaped/double-tuned; V/D nonmon: non-monotonically V-shaped/double-tuned; circ: circumscribed; comp: complex. Spatial representation B) and distribution in cortical subfields D) of the different binaural response types. EI: Excitatory/inhibitory; EE: Excitatory/excitatory; E0: Excitatory/non-responsive. Abbreviation of field names as in Fig. 1C.