Auditory Cortex: Multiple Fields, their Architectonics and Connections in the Mongolian Gerbil

Steffen, H.; Simonis, C.; Thomas, H.; Tillein, Jochen; Scheich, Henning

doi:10.1007/978-1-4684-1300-7_33

Cited by 12 publications

(9 citation statements)

References 11 publications

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“…1). The combined extent of these two fields determined electrophysiologically was found to coincide closely with the extent of specific anatomical features of cortex seen in the Nissl-stained material and reconstructed from it (see also Steffen et al, 1988). This cortex is characterized by cell-dense layers II-IV, a wide and cell-sparse layer V, and a cell-dense layer VI (Fig.…”

Section: Histological Correlationsupporting

confidence: 62%

Functional Organization of Auditory Cortex in the Mongolian Gerbil (Meriones unguiculatus). I. Electrophysiological Mapping of Frequency Representation and Distinction of Fields

Thomas

Tillein

Heil

et al. 1993

Eur J of Neuroscience

152

148

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The frequency representation within the auditory cortex of the anaesthetized Mongolian gerbil (Meriones unguiculatus) was studied using standard microelectrode (essentially multiunit) mapping techniques. A large tonotopically organized primary auditory field (AI) was identified. High best frequencies (BFs) were represented rostrally and low BFs caudally along roughly dorsoventrally oriented isofrequency contours. Additional tonotopic representations were found adjacent to AI. Rostral to AI was a smaller field with a complete tonotopic gradient reversed with respect to that in AI (mirror image representation) and was termed the anterior auditory field (AAF). BFs in the range from 0.1 to 43 kHz, apparently covering the hearing range of the Mongolian gerbil, were found in AI and AAF. Units in these two core fields responded to narrow frequency ranges with short latencies. Ventral to the common high-frequency border to AAF and AI, a rapid transition to very low BFs suggested the presence of a ventral field (V). Caudal to AI two small tonotopically organized fields were identified, a dorsoposterior field (DP) and a ventroposterior field (VP). The VP showed a tonotopic organization mirror imaged to that of AI, i.e. low frequencies were represented rostrally near the caudal border of AI, and high frequencies caudally. The DP showed a concentric frequency organization with high BFs located in the centre. Units in DP and VP fired less strongly, with considerably longer latencies, and responded to a broader range of frequencies than units in AI and AAF. Dorsocaudal to AI a dorsal field (D) was identified, harbouring units that responded to very broad ranges of frequencies. A tonotopic organization of field D could not be discerned. In the border region of AI and D, low-frequency responses were similar to those found in parts of AI and AAF, but without a clear-cut tonotopic organization. This region was termed Ald. The two core fields AI and AAF appeared to be located within the koniocortex, while the remaining fields lay outside. Our data show that the organization of the gerbil auditory cortex is highly elaborate, with parcellation into fields as complex as in cat or primates.

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Section: Histological Correlationsupporting

confidence: 62%

Functional Organization of Auditory Cortex in the Mongolian Gerbil (Meriones unguiculatus). I. Electrophysiological Mapping of Frequency Representation and Distinction of Fields

Thomas

Tillein

Heil

et al. 1993

Eur J of Neuroscience

152

148

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“…Previous 2DG studies in the cat, rat and gerbil either obtained weak labelling of the auditory cortex or bands of activity which were difficult to interpret (Hungerbuhler et al, 1981;Webster et al, 1978;Ryan et al, 1982;Gonzalez-Lima and Scheich, 1986). With respect to methodological aspects, however, the two latter studies lead the way to the present approach (see also Scheich et al, 1986;Steffen et al, 1988). Hungerbuhler et al (1981) found multiple dorsoventral bands in A1 of the cat stimulated with wide-band noise.…”

Section: Methodological Considerationsmentioning

confidence: 76%

“…The 2DG technique provides a rather complete spatial overview of stimulusspecific neuronal activity in a system. It could therefore be employed, even in combination with other neurobiological techniques (Steffen et al, 1988;Thomas, 1989), as a tool to address questions beyond simple tonotopicity, such as developmental changes (e.g. Heil and Scheich, 1992a) or lesion-(e.g.…”

Section: Introductionmentioning

confidence: 99%

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Functional Organization of Auditory Cortex in the Mongolian Gerbil (Meriones unguiculatus) II. Tonotopic 2‐Deoxyglucose

Scheich

Heil

Langner

1993

Eur J of Neuroscience

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The tonotopic organization of the auditory cortex in the Mongolian gerbil was mapped with 2-deoxyfluoro-D-glucose (2DG) using narrow-band frequency-modulated tones of different centre frequency (FM tones) and tones periodically alternating between two different frequencies (alternating tones) as stimuli. Continuous tone bursts of a constant frequency and repetition rate were used in initial experiments. Continuous tones produced 2DG patterns similar to those observed in animals that were not specifically stimulated. With tone bursts of constant frequency and repetition rate variable patterns were observed, some of which could be interpreted only in retrospect in the light of results obtained with FM tones and alternating tones. These stimuli, in contrast, produced differential metabolic responses which in conjunction with 2DG data from monaural animals and electrophysiological data made it possible to distinguish a primary auditory field AI with its dorsal region Ald, an anterior auditory field AAF, a ventral field V, a dorsoposterior field DP and a ventroposterior field VP, a dorsal field D, and in addition an anteroventral field AV. In the largest field (AI) and the smaller rostrally adjacent field AAF, frequency-specific dorsoventral bands of labelling (isofrequency contours) were mapped quantitatively. Bands shifted as a function of frequency relative to each other and to an independent spatial reference line in the lateral hippocampus. Spatial analysis of the single bands obtained with FM tones, and of the double bands obtained with alternating tones in both fields, revealed roughly mirror-imaged tonotopic maps of AI and AAF. In AI the progression from low to high frequencies was from caudal to rostral and in AAF the gradient was reversed, leading to a common high-frequency border of the two fields. In AI, the spatial resolution for frequencies below 16 kHz was in similar intervals per octave and higher for frequencies below 1 kHz. AI showed a somewhat higher spatial resolution for frequencies (at least below 1 kHz) as well as longer isofrequency contours than AAF. The 2-deoxyglucose patterns provided average tonotopic maps and topological data on various fields, as well as reliable landmarks in the gerbil's auditory cortex.

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“…Early electrophysiological investigations revealed a tonotopic arrangement of neuronal frequency preferences in A1 in all species studied, including monkeys 2 , cats 3 , ferrets 4 , gerbils 5 , and rats 6 . More recent multielectrode recordings 7–9 and large-scale imaging experiments 10 have confirmed the presence of a tonotopic gradient over large areas of A1 in carnivores and primates, while single-neuron recordings in awake animals have reported clear frequency gradients in marmosets 11 and weak tonotopy in cats 12 .…”

Section: Introductionmentioning

confidence: 99%

Complexity of frequency receptive fields predicts tonotopic variability across species

Gaucher

Panniello

Ivanov

et al. 2019

Preprint

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14Primary cortical areas contain maps of sensory features, including sound frequency in primary 15 auditory cortex (A1). Two-photon calcium imaging in mice has confirmed the presence of these large-16 scale maps, while uncovering an unexpected local variability in the stimulus preferences of individual 17 neurons in A1 and other primary regions. Here we show that fractured tonotopy is not unique to 18 rodents. Using two-photon imaging, we found that local variance in frequency preferences is 19 equivalent in ferrets and mice. Much of this heterogeneity was due to neurons with complex 20 frequency tuning, which are less spatially organized than those tuned to a single frequency. Finally, 21we show that microelectrode recordings may describe a smoother tonotopic arrangement due to a bias 22 towards neurons with simple frequency tuning. These results show that local variability in the 23 tonotopic map is not restricted to rodents and help explain inconsistencies in cortical topography 24 across species and recording techniques. 25 26 27 restricted to single neuron recordings, the spacing between neurons is typically ~100 µm or greater, so 56 local variations in stimulus preferences cannot be examined 24 . Second, multielectrode recordings may 57 be biased more towards the most robustly responding neurons in granular layers that receive direct 58 thalamic input, whereas most two-photon imaging studies have been restricted to the superficial layers 59 of the cortex 14,25 . However, Tischbirek et al. report similar tonotopic organization across all layers of 60 mouse auditory cortex 26 . Third, the variations in tonotopy across studies may partly reflect a species 61 difference in the cortical organization of rodents and higher mammals, particularly as local thalamic 62 inputs to A1 in mice are also heterogeneous in their frequency tuning 27 . Two-photon studies of 63 primary visual cortex have revealed poorer spatial organization of orientation tuning in rodents than in 64 cats 23,28 , tree shrews 29 , and ferrets 30 . The same may be true of tonotopy in A1. This view is further 65 supported by a recent study in marmosets, in which A1 was reported to be more tonotopically 66 organized than in rats 31 . 67 68 It is not clear how spatial organization of tuning to a single sound frequency coincides with the known 69 functions and complex frequency receptive fields of auditory cortex. Throughout the ascending 70 auditory pathway, neurons progressively integrate spectral and temporal features of sound 32 , and the 71 receptive fields of many A1 neurons are poorly predicted by a model of linear tuning to a single sound 72 frequency 33,34 . Recent studies have shown that the preferred frequencies of weakly tuned A1 neurons 73 are poorly mapped 20,26 . An outstanding question we address here is how neurons with reliable tuning 74 to multiple frequency peaks impact on tonotopic organization. 75 76The present experiments also examine whether local heterogeneity in tonotopy is a general feature of 77 mammalian A1, or a peculia...

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Auditory Cortex: Multiple Fields, their Architectonics and Connections in the Mongolian Gerbil

Cited by 12 publications

References 11 publications

Functional Organization of Auditory Cortex in the Mongolian Gerbil (Meriones unguiculatus). I. Electrophysiological Mapping of Frequency Representation and Distinction of Fields

Functional Organization of Auditory Cortex in the Mongolian Gerbil (Meriones unguiculatus). I. Electrophysiological Mapping of Frequency Representation and Distinction of Fields

Functional Organization of Auditory Cortex in the Mongolian Gerbil (Meriones unguiculatus) II. Tonotopic 2‐Deoxyglucose

Complexity of frequency receptive fields predicts tonotopic variability across species

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