Susanne Radtke-Schuller

A stereotaxic method for small animals using experimentally determined reference profiles.

In bats conventional stereotaxic methods do not yield sufficient positional accuracy to allow reliable recordings and tracer injections in subnuclei of the auditory system. In a newly developed stereotaxic system experimentally measured patterns of skull profile lines are used to define the animals brain position with an accuracy of +/- 100 microns. By combining the neurophysiological stereotaxic procedure with a standardization of the neuroanatomical processing of the brains, the location of recordings, stimulations or injections can be readily transformed into brain atlas coordinates. This facilitates the compilation and comparison of data within and among animals. The system is not restricted to use in bats and can be readily adapted to other experimental animals.

Adaptive, behaviorally gated, persistent encoding of task-relevant auditory information in ferret frontal cortex

Top-down signals from frontal cortex are thought to be important in cognitive control of sensory processing. To explore this interaction, we compared activity in ferret frontal cortex and primary auditory cortex (A1) during auditory and visual tasks requiring discrimination between classes of reference and target stimuli. Frontal cortex responses were behaviorally gated, selectively encoded the timing and invariant behavioral meaning of target stimuli, could be rapid in onset, and sometimes persisted for hours following behavior. These results are consistent with earlier findings in A1 that attention triggered rapid, selective, persistent, task-related changes in spectrotemporal receptive fields. Simultaneously recorded local field potentials revealed behaviorally gated changes in inter-areal coherence that were selectively modulated between frontal cortex and focal regions of A1 that were responsive to target sounds. These results suggest that A1 and frontal cortex dynamically establish a functional connection during auditory behavior that shapes the flow of sensory information and maintains a persistent trace of recent task-relevant stimulus features.

Facilitation and delay sensitivity of auditory cortex neurons in CF-FM bats, Rhinolophus rouxi and Pteronotus p.parnellii

Responses of auditory neurons to complex stimuli were recorded in the dorsal belt region of the auditory cortex of two taxonomically unrelated bat species, Rhinolophus rouxi and Pteronotus parnellii parnellii, both showing Doppler shift compensation behaviour. As in P.p.parnellii (Suga et al., J. Neurophysiol, 49, 1573–1626, 1983), cortical neurons of R. rouxi show facilitated responses to pairs of pure tones or frequency modulations. Best frequencies for the two components lie near the first and second harmonic of the echolocation call but are in most cases not harmonically related. Neurons facilitated by pairs of pure tones show little dependence on the delay between the stimuli, whereas pairs of frequency modulations evoke best facilitated responses at distinct best delays between 1 and 10 ms. Facilitated neurons are found in distinct portions of the dorsal cortical belt region, with a segregation of facilitated neurons responding to pure tones and to frequency modulations. Non‐facilitated neurons are found throughout the field. Neurons are topographically aligned with increasing best delays along a rostrocaudal axis. The best delays between 2 and 4 ms are largely overrepresented numerically, and occupy ˜56% of the cortical area containing facilitated neurons. A functional interpretation of the large overrepresentation of best delays ˜3ms is proposed. Facilitated neurons are located almost entirely within layer V of the dorsal field.

Neural control of vocalization in bats: mapping of brainstem areas with electrical microstimulation eliciting species-specific echolocation calls in the rufous horseshoe bat

Summary1. The functional role of brainstem structures in the emission of echolocation calls was investigated in the rufous horseshoe bat, Rhinolophus rouxi, with electrical low-current microstimulation procedures. 2. Vocalizations without temporal and/or spectral distortions could be consistently elicited at low threshold currents (typically below 10 μA) within three clearly circumscribed brainstem areas, namely, the deep layers and ventral parts of the intermediate layers of the superior colliculus (SC), the deep mesencephalic nucleus (NMP) in the dorsal and lateral midbrain reticular formation and in a distinct area medial to the rostral parts of the dorsal nucleus of the lateral lemniscus. The mean latencies in the three vocal areas between the start of the electrical stimulus and the elicited vocalizations were 47 msec, 38 msec and 31 msec, respectively. 3. In pontine regions and the cuneiform nucleus adjacent to these three vocal areas, thresholds for eliciting vocalizations were also low, but the vocalizations showed temporal and/or spectral distortions and were often accompanied or followed by arousal of the animal. 4. Stimulus intensity systematically influenced vocalization parameters at only a few brain sites. In the caudo-ventra1 portions of the deep superior colliculus the sound pressure level of the vocalizations systematically increased with stimulus intensity. Bursts of multiple vocalizations were induced at locations ventral to the rostral parts of the cuneiform nucleus. No stimulus-intensity dependent frequency changes of the emitted vocalizations were observed. 5. The respiratory cycle was synchronized to the electrical stimuli in all regions where vocalizations could be elicited as well as in more ventrally and medially adjacent areas not yielding vocalizations on stimulation. 6. The possible functional involvement of the “vocal” structures in the audio-vocal feedback system of the Dopplercompensating horseshoe bat is discussed.

The nuclei of the lateral lemniscus in the rufous horseshoe bat,Rhinolophus rouxi

Summary1.In the rufous horseshoe bat,Rhinolophus rouxi, responses to pure tones and sinusoidally frequency modulated (SFM) signals were recorded from 289 single units and 241 multiunit clusters located in the nuclei of the lateral lemniscus (NLL).2.The distribution of best frequencies (BFs) of units in all three nuclei of the lateral lemniscus showed an overrepresentation in the range corresponding to the constant-frequency (CF) part of the echolocation signal (‘filter frequency’ range): in the ventral nucleus of the lateral lemniscus (VNLL) ‘filter neurons’ represented 43% of all units encountered, in the intermediate nucleus (INLL) 33%, and in dorsal nucleus (DNLL) 29% (Fig. 2a). Neurons with best frequencies in the filter frequency range had highest Q10dB-values (maxima up to 400, Fig. 2c) and only in low-frequency units were values comparable to those found in other mammals. On the average, filter neurons in ventral nucleus had higher Q10dB-values (about 220) than did those in intermediate and dorsal nucleus (both about 160, Fig. 2d).3.Response patterns and tuning properties showed higher complexity in the dorsal and intermediate nucleus than in the ventral nucleus of the lateral lemniscus (Figs. 4 and 6). Multiple best frequencies were found in 12 neurons, nine of them with harmonically related excitation maxima (Fig. 5c, d). Best frequencies of six of these harmonically tuned units could not be correlated with any harmonic components of the echolocation signal. Half of all multiple tuned neurons were located in the caudal dorsal nucleus the other half in the caudal intermediate nucleus.4.Synchronization of responses to sinusoidally frequency modulated (SFM) signals occurred in VNLL-units in the average up to modulation frequencies of 515 Hz (maximum about 800 Hz) whereas in the intermediate and dorsal nucleus of the lateral lemniscus responses were synchronized in the average only up to modulation frequencies of about 300 Hz (maximum about 600 Hz) (Figs. 7 and 8).5.A tonotopic arrangement of units was found in the intermediate nucleus of the lateral lemniscus with units having high best frequencies located medially and those with low best frequencies laterally. In the dorsal nucleus the tonotopic distribution was found to be fairly similar to that in the intermediate nucleus but much less pronounced. In more rostral parts of the dorsal nucleus additionally higher best frequencies predominated whereas in caudal areas of that nucleus and also of the intermediate nucleus low BFs were found more regularly. The ventral nucleus of the lateral lemniscus was characterized by a remarkably high proportion of neurons having best frequencies in the filter frequency range. In fact, the entire lateral, central and dorsomedial parts were devoted to the representation of the filter frequency. Lower best frequencies were present only in the medial parts of the ventral nucleus of the lateral lemniscus (Fig. 9).

Emergent selectivity for task-relevant stimuli in higher-order auditory cortex

A variety of attention-related effects have been demonstrated in primary auditory cortex (A1). However, an understanding of the functional role of higher auditory cortical areas in guiding attention to acoustic stimuli has been elusive. We recorded from neurons in two tonotopic cortical belt areas in the dorsal posterior ectosylvian gyrus (dPEG) of ferrets trained on a simple auditory discrimination task. Neurons in dPEG showed similar basic auditory tuning properties to A1, but during behavior we observed marked differences between these areas. In the belt areas, changes in neuronal firing rate and response dynamics greatly enhanced responses to target stimuli relative to distractors, allowing for greater attentional selection during active listening. Consistent with existing anatomical evidence, the pattern of sensory tuning and behavioral modulation in auditory belt cortex links the spectrotemporal representation of the whole acoustic scene in A1 to a more abstracted representation of task-relevant stimuli observed in frontal cortex.

Auditory Cortex of the Rufous Horseshoe Bat: 1. Physiological Response Properties to Acoustic Stimuli and Vocalizations and the Topographical Distribution of Neurons

The extent and functional subdivisions of the auditory cortex in the echolocating horseshoe bat, Rhinolophus rouxi, were neurophysiologically investigated and compared to neuroarchitectural boundaries and projection fields from connectional investigations. The primary auditory field shows clear tonotopic organization with best frequencies increasing in the caudorostral direction. The frequencies near the bats resting frequency are largely over‐represented, occupying six to 12 times more neural space per kHz than in the lower frequency range. Adjacent to the rostral high‐frequency portion of the primary cortical field, a second tonotopically organized field extends dorsally with decreasing best frequencies. Because of the reversed tonotopic gradient and the consistent responses of the neurons, the field is comparable to the anterior auditory field in other mammals. A third tonotopic trend for medium and low best frequencies is found dorsal to the caudal primary field. This area is considered to correspond to the dorsoposterior field in other mammals. Cortical neurons had different response properties and often preferences for distinct stimulus types. Narrowly tuned neurons (Q10dB < 20) were found in the rostral portion of the primary field, the anterior auditory field and in the posterior dorsal field. Neurons with double‐peaked tuning curves were absent in the primary area, but occurred throughout the dorsal fields. Vocalization elicited most effectively neurons in the anterior auditory field. Exclusive response to pure tones was found in neurons of the rostral dorsal field. Neurons preferring sinusoidal frequency modulations were located in the primary field and the anterior and posterior dorsal fields adjacent to the primary area. Linear frequency modulations optimally activated only neurons of the dorsal part of the dorsal field. Noise‐selective neurons were found in the dorsal fields bordering the primary area and the extreme caudal edge of the primary field. The data provide a survey of the functional organization of the horseshoe bats auditory cortex in real coordinates with the support of cytoarchitectural boundaries and connectional data.

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

BackgroundThe 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).ResultsThe auditory cortical area of P. discolor is located at parieto-temporal portions of the neocortex. It covers a rostro-caudal range of about 4800 μm and a medio-lateral distance of about 7000 μm 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.ConclusionThe 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.

Cortical connections of the claustrum and subjacent cell groups in the hedgehog tenrec

Cyto- and chemoarchitectural findings have recently suggested that in the hedgehog tenrec, the claustrum is not located below but between the layers of the rhinal/insular cortex (Künzle and Radtke-Schuller 2000b). The present connectional study confirms this unusual position. Tracer injections were made into various isocortical and allocortical regions. They showed that the tenrec’s dorsal claustrum was reciprocally and bilaterally connected with the neocortex. The ventral claustrum was connected with mainly the ipsilateral paleocortex, additionally with the ventromedial frontal cortex and possibly the subiculum. A sparsely labeled cell group separated the claustrum from the labeled cells located in the depth of the RCx and the adjacent paleo- and neocortices. On the basis of the linear arrangement of these latter cells immediately adjacent to the subcortical white matter, and the restriction of their labeling to the ipsilateral side, one might interpret preliminarily these cells as layer 6B cells or persisting subplate neurons. Their cortical projections showed a similar topographic organization as the claustro-cortical projections. The unusual features described in tenrec were discussed with respect to similar organizations in other mammals with poorly differentiated brains and compared with embryonic brains of mammals with more differentiated brains.

Cytoarchitecture of the medial geniculate body and thalamic projections to the auditory cortex in the rufous horseshoe bat (Rhinolophus rouxi)

The auditory cortex in echolocating bats is one of the best studied in mammals, yet the projections of the thalamus to the different auditory cortical fields have not been systematically analyzed in any bat species. The data of the present study were collected as part of a combined investigation of physiological properties, neuroarchitecture, and chemoarchitecture as well as connectivity of cortical fields in Rhinolophus in order to establish a neuroanatomically and functionally coherent view of the auditory cortex in the horseshoe bat. This paper first describes the neuroanatomic parcellation of the medial geniculate body and then concentrates on the afferent thalamic connections with auditory cortical fields of the temporal region. Deposits of horseradish peroxidase and wheatgerm-agglutinated horseradish peroxidase were made into neurophysiologically characterized locations of temporal auditory cortical fields; i.e., the tonotopically organized primary auditory cortex, a ventral field, and a temporal subdivision of a posterior dorsal field. A clear topographic relationship between thalamic subdivisions and specific cortical areas is demonstrated. The primary auditory cortex receives topographically organized input from the central ventral medial geniculate body. The projection patterns to the temporal subdivision of the posterior dorsal field suggest that it is a “core” field, similar to the posterior fields in the cat. Projections to the ventral field arise primarily from border regions of the ventral medial geniculate body. On the whole, the organization of the medial geniculate body projections to the temporal auditory cortex is quite similar to that described in other mammals, including cat and monkey.