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

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 Aid, 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.     

Grating acuity of the Mongolian gerbil (Meriones unguiculatus)

The grating acuity of the Mongolian gerbil was measured using a two-alternative forced-choice task in a jumping stand. Frequency-of-seeing curves generated by a modified method of limits indicated that the acuity of the gerbil for a horizontal square-wave grating is about 1.5-2.0 cycles/degree (c/deg) at 70 cd/m2, using the 70%- and 80%-correct levels of performance as criteria for defining acuity. The acuity for horizontal gratings is reliably better than that for vertical gratings, and this difference does not appear to be luminance-dependent. A corresponding orientation anisotropy is not seen in acquisition scores, nor is an 'oblique effect' evident. The acuity of the gerbil continues to increase with luminance into the (human) photopic range, suggesting the existence of a functional cone system. The gerbil visual system appears to be well adapted for detail vision in a diurnal lifestyle.     

Eye and brain growth in the Mongolian gerbil (Meriones unguiculatus)

Eye and brain growth were evaluated by measures of weight and surface dimensions at 11 ages spanning the period from birth to 150 days of age in the Mongolian gerbil (Meriones unguiculatus). Brain weight was found to increase very rapidly until day 18, followed by a more gradual increase to asymptote by 70 days of age. Eye growth follows overall body growth more closely than brain growth. Eye shape was found to change from ovoid to spherical over the first 70 days of life. The possible relationship between eye growth and retinal specialization is considered, and brain growth is compared across several rodent species.     

The development of visual acuity in the Mongolian gerbil (Meriones unguiculatus)

The development of visual acuity for vertically oriented gratings was followed in gerbil pups from 34 days of age until adulthood using a jumping stand procedure. Acuity was found to improve gradually from an initial level of about 0.7 cycles/degree to asymptotic values of 1.2-1.6 cycles/degree by 70 days of age. Acuity did not vary as a function of viewing distance over the range tested (17.5-46 cm). Practice was found to play some role in the acuity changes seen but cannot alone explain the results. The contributions of other performance variables and of neural development are considered.     

Stereotaxic atlas of the hypothalamus of the Mongolian gerbil (Meriones unguiculatus)

A stereotaxic atlas of the hypothalamic area of the Mongolian gerbil (Meriones unguiculatus) is presented along with medical coordinates for all primary nuclei and the third ventricle.     

Certain efferent cortical fiber pathways of the Mongolian gerbil (Meriones unguiculatus)

Three areas of responsive cortex were demonstrated by electrical stimulation in the gerbil. Low voltage stimulation of frontal areas yielded a sequential pattern of discrete contralateral movements. Proceeding from a rostroventral to a caudodorsal position facial movements were obtained followed by upper extremity, trunk and lower extremity movements. This area includes primary motor cortex (area 4) in the gerbil. A comparable rostrocaudal motor pattern was obtained by stimulation above the rhinal fissure (insular cortex) and also from certain parietal areas. Although the sequential motor pattern was obvious in these additional areas of excitable cortex, the movements were more generalized and slightly higher voltages were required to obtain satisfactory results. A series of destructive lesions were made in each of these cortial areas. Subsequent degeneration studies, using reduced silver techniques, revealed that frontal and parietal cortex gave rise to corticospinal fibers. In addition all three areas gave rise to fibers which coursed to certain extrapyramidal nuclei of the basal ganglia, ventral thalamus, midbrain tegmentum, and medullary reticular formation.     

Transection of the pineal stalk produces convulsions in male Mongolian gerbils (Meriones unguiculatus)

The pineal gland has been implicated in the regulation of epileptic-like seizures in gerbils. Pinealectomy of gerbils results in seizures which affect approximately 80% of the gerbils. Telencephalic catecholamine levels are depressed by pinealectomy in gerbils and it has been suggested that the reduced norepinephrine (NE) levels are responsible for initiating or facilitating these seizures. The present study found that pineal stalk transection produced convulsions in gerbils which were indistinguishable from pinealectomy-induced convulsions. Stalk transection also produced a depression (38%) in parietal cortex NE levels which was similar to a depression observed in pinealectomized gerbils (52%). These depressions in cortical NE levels were not observed in other brain regions, specifically the hippocampus or the amygdala. However, a decline (25%) in hypothalamic NE levels was observed after stalk transection. These results suggest that the signals responsible for pinealectomy-induced convulsions are carried by the pineal stalk and that pinealectomy produces regional, not global, reductions in NE content.     

Opiate receptor binding in the brain of the seizure sensitive Mongolian gerbil (Meriones unguiculatus)

Opiate receptor binding was studied in seizure sensitive (SS) and seizure resistant (SR) strains of the Mongolian gerbil. Cryostat sections of the brain were labeled with [3H]-dihydromorphine, subjected to autoradiography and analysed by microdensitometry. SS gerbils, prior to seizure induction, demonstrated overall greater brain opiate binding when compared to SR animals. Immediately following a seizure, binding in the interpeduncular nucleus fell to levels found in SR animals. The increased opiate binding in the SS (pre-seizure) compared to SR gerbils could reflect a deficit of endogenous ligand which could underlie the seizure diathesis in the gerbil.     

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

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 Aid. 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.     

The ontogenesis of sensorimotor reflexes in the Mongolian gerbil Meriones unguiculatus.

The ontogeny of a number of sensorimotor reflexes has been studied in the Mongolian gerbil. In contrast to a number of other mammals, the gerbil has relatively long and strong hindlimbs but small forelimbs, indicating their different importance for a number of locomotor acts, and during the developmental period studied, the hindlimbs grow at a much faster rate than the forelimbs. The following sequence of appearance and maturation of the reflexes was observed: rooting, forelimb hopping, surface body righting, forelimb grasp, hindlimb hopping, chin tactile placing, visual placing, air body righting and, at the same time, forelimb and hindlimb tactile placing. This sequence concords with the general gradient of development and maturation of the spinal and brain centers subserving these reflexes, as evaluated from Nissl preparations. The results indicate that there is no clearcut rostro-caudal gradient of postnatal maturation of the spinal cord and the spinally mediated reflexes, but that there is a general caudo-rostral gradient of brain maturation and of the brain-mediated reflexes. Comparisons with other mammals are made.     

Diurnal variation of c-Fos expression in subdivisions of the dorsal raphe nucleus of the Mongolian gerbil (Meriones unguiculatus).

Recent studies suggest that the dorsal raphe nucleus (DRN) of the brainstem contains several subdivisions that differ both anatomically and neurochemically. The present study examined whether variation of c-Fos expression across the 24-hour light-dark cycle may also be different in these subdivisions. Animals were kept on a 12:12 light-dark cycle, were perfused at seven different time points, and brain sections were processed by using c-Fos immunocytochemistry. At all coronal levels of the DRN, c-Fos expression reached a peak 1 hour after the light-dark transition (lights-off) and reached its lowest levels in the middle of the light period. In contrast to the light-dark transition, c-Fos levels did not change significantly after the dark-light transition (lights-on). One-way analysis of variance (ANOVA) revealed that the diurnal variation of c-Fos expression was highly significant in the caudal ventral DRN. Similar variation in c-Fos expression also was observed in the other DRN subdivisions, but this variation appeared to gradually diminish in the caudal-to-rostral and ventromedial-to-dorsomedial directions. Double-label immunocytochemistry revealed that, 1 hour after lights-off, only 11% of c-Fos-positive neurons in the caudal ventral DRN were serotonin (5-HT)-immunoreactive. These results suggest that DRN subdivisions may differ functionally with regard to the diurnal cycle, and that these differences may be reflected in the activity of nonserotonergic cells in the DRN.     

The Mongolian gerbil (Meriones unguiculatus) as a model for the study of the epilepsies: EEG records of seizures.

EEG recordings have been made from freely moving, seizure sensitive gerbils during seizures of varying severity. The localization of seizure activity in various brain areas and the generalization of this activity could be correlated with the observed motor manifestations. Paroxysmal observed motor manifestations. Paroxysmal bursting has also been recorded in the parietal cortex of a xeizure sensitive animal in which no concomitant peripheral motor activity was evident. These observations strengthen the suggestion that selectively bred epileptic strains of Meriones unguiculatus may be a suitable animal model for the study of the epilepsies.     

The effects of posterior cortical lesions on responses to visual threats in the Mongolian gerbil (Meriones unguiculatus).

Mongolian gerbils received aspiration lesions of either primary visual cortex (PVC), medial extrastriate visual cortex, retrosplenial cortex (RSC), or sham operations. The responses of gerbils to the presentation of an overhead visual stimulus were recorded in an open field. In all groups, presentation of the stimulus produced an increase in rearing. This suggests that the stimulus was detected by all animals. Gerbils with RSC or PVC lesions showed reduced levels of response to the stimulus. We suggest that some of the observed deficits can be explained as failures to produce responses to threat that are appropriate to the context in which the the threat was presented.     

Topographic organization of serotonergic dorsal raphe neurons projecting to the superior colliculus in the Mongolian gerbil (Meriones unguiculatus).

Recent evidence suggests that the dorsal raphe nucleus (DRN) of the brainstem is a collection of neuronal clusters having different neurochemical characteristics and efferent projection patterns. To gain further insight into the neuroanatomic organization of the DRN, neuronal populations projecting to the superior colliculus (SC) were mapped in a highly visual rodent, the Mongolian gerbil (Meriones unguiculatus). Retrograde tracers Fluoro-Gold (FG) or cholera toxin subunit-B (CTB) were injected into the superficial layers of the SC, and serotonin (5-hydroxytryptamine, 5-HT) -positive cells were identified by using immunocytochemistry in the FG-injected animals. Based on its projections to the SC, the DRN was divided into five rostrocaudal levels. In the rostral and middle levels of the DRN, virtually all FG-filled cells occurred in the lateral DRN, and 36-55% of 5-HT-immunoreactive (5-HT-ir) cells were also double-labeled with FG. Caudally, FG-filled cells occurred in the lateral, ventromedial, and interfascicular DRN; and 44, 12, and 31% of 5-HT-ir cells, respectively, were also FG-filled. The dorsomedial DRN contained only a small proportion of FG-filled cells at its most caudal level and was completely devoid of FG-filled cells more rostrally. The CTB-injected animals showed a similar distribution of retrogradely labeled cells in the DRN. Topographically, the dorsal tegmental nucleus and the laterodorsal tegmental nucleus appeared to be closely associated with 5-HT-ir cells in the caudal DRN. These results suggest that the lateral DRN and the ventromedial/interfascicular DRN may be anatomically, morphologically, and neurochemically unique subdivisions of the gerbil DRN.     

Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). III. Anatomical subdivisions and corticocortical connections

The auditory cortex of the Mongolian gerbil comprises several physiologically identified fields, including the primary (AI), anterior (AAF), dorsal (D), ventral (V), dorsoposterior (DP) and ventroposterior (VP) fields, as established previously with electrophysiological [Thomas et al. (1993) Eur. J. Neurosci., 5, 882] and functional metabolic techniques [Scheich et al. (1993) Eur. J. Neurosci., 5, 898]. Here we describe the cyto-, myelo- and chemoarchitecture and the corticocortical connections of the auditory cortex in this species. A central area of temporal cortex corresponding to AI and the rostrally adjacent AAF is distinguished from surrounding cortical areas by its koniocortical cytoarchitecture, by a higher density of myelinated fibres, predominantly in granular and infragranular layers, and by characteristic patterns of immunoreactivity for the calcium-binding protein parvalbumin (most intense staining in layers III/IV and VIa) and for the cytoskeletal neurofilament protein (antibody SMI-32; most intense staining in layers III, V and VI). Concerning the cortical connections, injections of the predominantly anterograde tracer biocytin into the four tonotopically organized fields AI, AAF, DP and VP yielded the following labelling patterns. (i) Labelled axons and terminals were seen within each injected field itself. (ii) Following injections into AI, labelled axons and terminals were also seen in the ipsilateral AAF, DP, VP, D and V, and in a hitherto undescribed possible auditory field, termed the ventromedial field (VM). Similarly, following injections into AAF, DP and VP, labelling was also seen in each of the noninjected fields, except in VM. (iii) Each field projects to its homotopic counterpart in the contralateral hemisphere. In addition, field AI projects to contralateral AAF, DP and VP, field DP to contralateral AI and VP, and field VP to contralateral AI and DP. (iv) Some retrogradely filled pyramidal neurons within the areas of terminal labelling indicate reciprocal connections between most fields, both ipsilateral and contralateral. (v) The labelled fibres within the injected and the target fields, both ipsilateral and contralateral, were arranged in continuous dorsoventral bands parallel to isofrequency contours. The more caudal the injection site in AI the more rostral was the label in AAF. This suggests divergent but frequency-specific connections within and, at least for AI and AAF, also across fields, both ipsilateral and contralateral. (vi) Projections to associative cortices (perirhinal, entorhinal, cingulate) and to other sensory cortices (olfactory, somatosensory, visual) from AAF, DP and VP appeared stronger than those from AI. These data support the differentiation of auditory cortical fields in the gerbil into at least 'core' (AI and AAF) and 'noncore' fields. They further reveal a complex pattern of interconnections within and between auditory cortical fields and other cortical areas, such that each field of auditory cortex has its unique set of connections.