Constraints on the coding of sound frequency imposed by the avian interaural canal

Extracellular recordings were made from the midbrain auditory area to determine the limits of auditory frequency sensitivity in a variety of birds. The audiograms of some species show a consistent missing frequency range of 1/3 to 1/2 an octave, to which no neurons are tuned. All species, except owls, have a low upper frequency limit in comparison with mammals of similar headwidth. A consideration of both the upper frequency limits and the missing frequency ranges led to the conclusion that frequencies which do not generate localization cues are not represented in the midbrain. The upper frequency limit appears to match the upper limit of generation of significant interaural and monaural intensity cues to localization. The variation of these cues with frequency was examined through a simple model of the birds' sound receiving system which incorporated the interaural canal and considered the tympanic membranes as pressure difference receivers. Apart from coraciiform species, which have low upper frequency limits matching the frequency of the primary missing frequency band of other species, and owls, which have high upper frequency limits, the upper frequency limits of the birds studied are inversely related to head-width. The argument for missing frequency ranges being related to nonlocalizable frequencies is simpler, for it has been found previously, using cochlear microphonic recording, that within a bird's audiogram there are frequency regions with poor directionality cues. These regions appear to correspond to the missing frequency ranges

Acute changes in cutaneous receptive fields in primary somatosensory cortex after digit denervation in adult flying fox

Acute effects of permanent and temporary denervation of the flying fox thumb were examined to test the hypothesis that a large area of skin around the cutaneous receptive field of multi-units (MRF) at a locus in primary somatosensory cortex (SI) supplies viable inputs which can be rapidly unmasked by interruption of the dominant input from the area of the MRF. The immediate effect of amputation of the thumb at loci where the original receptive field was entirely removed was to produce large MRFs on adjacent body areas (wrist, forearm, prowing, and finger membranes). Greatly expanded MRFs were also produced when amputation removed only part of the original MRF at a cortical locus. The probable source of input to account for the new receptive fields is the extensive arborization of ascending projections within the somatosensory pathway, which supply a cortical locus with a potential input from a far larger area than is represented in its normal receptive field. The rapidity with which new or expanded fields are seen following denervation indicates that the normally unexpressed inputs around a receptive field are not only potential inputs but are inherently viable. Hence the most likely explanation for the results of this study is that the effect of the denervation is to disrupt an inhibitory influence that normally has the role of shaping the receptive field. Temporary anesthesia of all or part of a MRF produced similar initial effects to amputation. When responsiveness returned to the locally anesthetized area (after 10-30 min), an expanded MRF persisted for a short time after which the boundaries of the MRF shrank. This rapid reversal suggests that a mechanistic rather than a plastic change is the basis for the acute effect of a small denervation on SI

C-fibres provide a source of masking inhibition to primary somatosensory cortex

Capsaicin was applied to the exposed radial nerve of adult flying foxes (n = 5) and cats (n = 2) while recording in primary somatosensory cortex froma single neuron with a receptive field on digits 1 or 2. Within four minutes of application of capsaicin the borders of these receptive fields dramatically expanded. In a further four flying foxes it was shown, with subcutaneous delivery just proximal to the receptive fields, that capsaicin need affect only afferents from the region of a neuron's receptive field to induce expansion. Capsaicin applied directly to a nerve, or subcutaneously in high concentrations, is a selective neurotoxin that rapidly prevents the propagation of action potentials in most C-fibres. The result provides a partial explanation for experiments involving the specific and complete denervation of receptive fields of neurons in primary somatosensory cortex. Such denervation does not lead to unresponsiveness but to immediate sensitivity to stimulation of areas surrounding the original fields. Thus it appears that some subclass of capsaicin-sensitive C-fibres provides a primary source for the masking inhibition that normally limits the extent of the receptive fields of cortical neurons

Interhemispheric transfer of plasticity in the cerebral cortex

Each half of the body surface is represented topographically in the contralateral cerebral hemisphere. Physiological data are presented showing that homotopic regions of primary somatosensory cortex are linked such that plasticity induced in one hemisphere, in the form of receptive field expansion brought about by a small peripheral denervation, is immediately mirrored in the other hemisphere. Neurons which display the plasticity show no responsiveness to stimulation of the ipsilateral body surface. This suggests that the pathways and mechanisms mediating this transfer are specific to the role of maintaining balance, or integration, between corresponding cortical fields

Interhemispheric modulation of somatosensory receptive fields: Evidence for plasticity in primary somatosensory cortex

Extracellular recordings were made from single and multiple neurons in primary somatosensory cortex (area 3b) of macaque monkeys and flying foxes. When a smell region of area 3b (or adjacent area 1) in the opposite hemisphere was cooled, thereby blocking activity that is normally transferred via the corpus callosum, larger receptive fields (RFs) were immediately unmasked for most neurons. RF expansion presumably reflects the expression of afferent inputs that are normally inhibited, suggesting that callosal inputs provide a source of tonic inhibition that contributes to the shaping of neuronal RFs. Quantitative analyses of single neuron responses revealed other effects that were consistent with a release from inhibition, such as increases in response magnitude to stimulation of points within the original RF and decreases in response latency. An unexpected finding was the reversal of these unmasking effects with extended periods of cooling: RFs returned to their original dimensions and within-field response magnitude decreased. In contrast to the initial effects, this reversal of disinhibition cannot be readily explained by an unmasking of previously unexpressed inputs. Any explanation for the reversal requires an increase in the efficacy of interneuron-mediated inhibition, and presumably occurs in response to ongoing, altered patterns of activity

Somatosensory cortical representation in the Australian ghost bat, Macroderma gigas

Bats of the two suborders Microchiroptera and Megachiroptera have a modified hand in which the digits of the forelimb are caudally oriented to form the wing. In a previous study of a megachiropteran species, this modification of body plan was found to be reflected in the somatosensory cortical representation such that the orientation of the digit representation was reversed compared with walking mammals. This finding suggests that the precisedetails of arrangement of topographical maps are functionally significant and do not merely reflect an order imposed by peripheral innervation. Recentevidence for separate origins of Microchiroptera and Megachiroptera raises the question of whether the cortical somatosensory representation in Microchiroptera will also have a reversal of digit orientation compared with walking mammals. We recorded multiunit activity from the somatosensory cortex of a microchiropteran bat, Macroderma gigas. We found two orderly representations of the body surface, SI and SII, in both of which the digit orientation was opposite to the head orientation in accordance with adaptation for flight, and reversed with respect to equivalent maps in other mammals. We also found minor variations in body surface representation compared with Megachiroptera, in line with their proposed independent evolution

Neuronal composition and morphology in layer IV of two vibrissal barrel subfields of rat cortex

The technique of intracellular injection in fixed, flattened slices was used to study neuronal composition and morphology in the postero-medial barrel subfield (PMBSF) and the antero-lateral barrel subfield (ALBSF) in layer IV of rat cortex. The PMBSF and the ALBSF contain the cortical representation of the mystacial and rostral snout vibrissae respectively. Neuronal composition differed between the PMBSF and the ALBSF. Modified pyramidal cells were the most numerous neuronal type in the PMBSF (73.1%), whereas spiny multipolar (stellate) neurons were the most numerous type in the ALBSF (40.9%). Tangential dendritic field areas of modified pyramidal cells and spiny multipolar cells in the barrels of the two barrel subfields were compared. Dendritic field areas of spiny multipolar neurons located in the barrels of the PMBSF and the ALBSF were similar (mean +/- SD; 2.44 +/- 1.83 x 10(4) and 2.88 +/- 1.47 x 10(4) microns2 respectively). Likewise, there was no significant difference in 'basal' dendritic field area of modified pyramidal neurons located in the barrels of the two different barrel subfields (4.63 +/- 1.96 x 10(4) and 4.45 +/- 1.81 x 10(4) microns2 for PMBSF and ALBSF respectively). The mean cross-sectional area of PMBSF barrels (20.5 +/- 5.69 x 10(4) microns2) in which neurons were injected was approximately seven times larger than that of the ALBSF (2.94 +/- 1.46 x 10(4) microns2). Thus, on average, the dendritic territories of these two neuronal classes sample a larger proportion of the cross-sectional area of the barrels in the ALBSF than in the PMBSF. We conclude that the close relationship between basal dendritic field area of supragranular pyramidal neurons and module size, reported in studies of other sensory areas, is not evident in all barrel subfields of the rat

Connections of somatosensory cortex in megachiropteran bats: The evolution of cortical fields in mammals

The cortical connections of the primary somatosensory area (SI or 3b), a caudal somatosensory field (area 1/2), the second somatosensory area (SII), the parietal ventral area (PV), the ventral somatosensory area (VS), and the lateral parietal area (LP) were investigated in grey headed flying foxes by injecting anatomical tracers into electrophysiologically identified locations in these fields. The receptive fields for clusters of neurons were mapped with sufficient density for injection sites to be related to the boundaries of fields, and to representations of specific body parts within the fields. In all cases, cortex was flattened and sectioned parallel to the cortical surface. Sections were stained for myelin and architectonic features of cortex were related to physiological mapping and connection patterns. We found patterns of topographic and nontopographic connections between 3b and adjacent anterior parietal fields 3a and 1/2, and fields caudolateral to 3b (SII and PV). Area 1/2 had both topographic and nontopographic connections with 3b, PP, and SII. Connections of SII and PV with areas 3b, 3a, and 1/2 were roughly topographic, although there was clear evidence for nontopographic connections between these fields. SII was most densely connected with area 1/2, while PV was most densely connected with 3b. SII had additional connections with fields in lateral parietal cortex and with subdivisions of motor cortex. Other connections of PV were with subdivisions of motor cortex and pyriform cortex. Laminar differences in connection patterns of SII and PV with surrounding cortex were also observed. Injections in the ventral somatosensory area revealed connections with SII, PV, area 1/2, auditory cortex, entorhinal cortex, and pyriform cortex. Finally, the lateral parietal field had very dense connections with posterior parietal cortex, caudal temporal cortex, and with subdivisions of motor cortex. Our results indicate that the 3b region is not homogeneous, but is composed of myelin dense and light regions, associated with 3b proper and invaginations of area 1/2, respectively. Connections of myelin dense 3b were different from invaginating portions of myelin light area 1/2. Our findings that 3b is densely interconnected with PV and moderately to lightly interconnected with SII supports the notion that SII and PV have been confused across mammals and across studies. Our connectional evidence provides further support for our hypothesis that area 1/2 is partially incorporated in 3b and has led to theories of the evolution of cortical fields in mammals

Monocular focal retinal lesions induce short-term topographic plasticity in adult cat visual cortex

Electrophysiological recording in primary visual cortex (V1) was performed both prior to and in the hours immediately following the creation of a discrete retinal lesion in one eye with an argon laser. Lesion projection zones (LPZs; 21-64 mm) were defined in the visual cortex by mapping the extent of the lesion onto the topographic representation in cortex. There was no effect on neuronal responses to the unlesioned eye or on its topographic representation. However, within hours of producing the retinal lesion, receptive fields obtained from stimulation of the lesioned eye were displaced onto areas surrounding the scotoma and were enlarged compared with the corresponding field obtained through the normal eye. The proportion of such responsive recording sites increased during the experiment such that 8-11 hours post-lesion, 56% of recording sites displayed neurons responsive to the lesioned eye. This is an equivalent proportion to that previously reported with long-term recovery (three weeks to three months). Responsive neurons were evident as far as 2.5 mm inside the border of the LPZ. The reorganization of the lesioned eye representation produced binocular disparities as great as 15°, suggesting interactions between sites in V1 up to 5.5 mm apart