R. F. Mark

Patterned neural activity in brain stem auditory areas of a prehearing mammal, the tammar wallaby (Macropus eugenii)

Is patterned neural activity in immature, prefunctioning sensory systems a general phenomenon? Such patterning has been found in the prenatal visual and somatosensory systems. We have now identified patterning in the immature auditory system of a prehearing mammal, the tammar wallaby. Neurones recorded in vivo from the eighth nerve and cochlear nucleus at pouch days 94-122 discharged in bursts with rhythmic inter-spike intervals. Our findings are applied to the argument that neural activity is vital to sensory development.

Australian marsupials as models for the developing mammalian visual system

This article makes two points. First, the diprotodont marsupials, including the kangaroos, wallabies and the Australian possum are not primitive mammals, and their brains make as good a general model of the higher mammals such as monkeys and humans as do those of the more common laboratory mammals such as cats and rats. Second, the peculiarities of marsupial reproduction, which comprises a very short period of intrauterine development, followed by a relatively protracted period of development in the pouch, provide unparalleled advantages for research into mammalian neuroembryology. Examples will be provided of how such research has made a contribution to our understanding of neural development, concentrating primarily on the visual system.

Retinotectal reorganization in goldfish—II. Effects of partial tectal ablation and constant light on the retina

Abstract In a proportion of small fish, after removal of half the tectum, exposure to constant light induces compression of the retinotectal projection. In contrast, it prevents compression in large fish. Loss of rod photoreceptors occurs in both small and large fish kept in constant light. This was not sufficient to induce compression. In large fish removal of half the tectum followed by exposure either to light/dark or to constant light has no consistent effect on the number of retinal ganglion cells. In small fish the removal of half the tectum alone causes a loss of ganglion cells in the eye projecting to the operated tectum. This in itself was not associated with compression. In half the small fish, exposure to constant light following the removal of half the tectum produced an even greater loss of ganglion cells in the eye projecting to the operated tectum. This increased loss of ganglion cells may be sufficient to induce compression, probably by creating vacant synaptic sites in the tectum. That only a proportion of fish show increased loss of cells correlates with the finding that only a proportion undergo compression in constant light.

VISUAL ACUITY, CONTRAST SENSITIVITY AND RETINAL MAGNIFICATION IN A MARSUPIAL, THE TAMMAR WALLABY (MACROPUS EUGENII

Abstract The visual acuity of the tammar wallaby was estimated using a behavioural discrimination task. The wallabies were trained to discriminate a high-contrast (86%) square-wave grating from a grey field of equal luminance (1000–6000 cd m−2). Visual-evoked cortical potentials were used to measure the complete contrast sensitivity function. The stimulus was a sinusoidal phase reversal of a sinusoidally modulated grating of various spatial frequencies and contrasts with a mean luminance of 40 cd m−2. The behavioural acuity was estimated to be about 4.8 cycles/deg. The contrast sensitivity peaked at about 0.15 cycles/deg and declined towards both lower and higher spatial frequencies. The cut-off frequency of the contrast sensitivity function is slightly lower than the behaviourally measured acuity at about 2.7 cycles/deg. The retinal magnification factor was estimated anatomically from laser lesions to be about 0.16 mm/deg. Based on the known ganglion cell density and the retinal magnification factor, an anatomical upper limit to visual acuity of about 6 cycles/deg can be calculated. The differences in estimates of visual acuity between the behavioural and anatomical methods on the one side and physiology on the other side are discussed.

Development of whisker representation in the cortex of the tammar wallaby Macropus eugenii

The somatosensory cortex associated with the whiskers has been studied in adult tammar wallabies (Macropus eugenii) and in pouch young from 60-120 days of pouch life. The time course of anatomical changes examined with succinic dehydrogenase (SDH) histochemistry and Nissl staining has been correlated with the maturation of electrically evoked cortical responses to stimulation of the whisker follicles. The earliest signs of aggregates of SDH reaction product in layer IV of the cortex were seen at 85 days, coincident with the first recordings of an immature cortical evoked potential. Aggregates, in a pattern corresponding to that of the facial whiskers, were most clearly seen from 90-140 days. At later stages, and in the adult, they were present but their arrangement was less clearly seen. By 186 days the electrical activity resembled the mature pattern. Patches of SDH activity in layer IV were not associated with changes in soma density characteristic of true barrels.

Two stages in the development of a mammalian retinocollicular projection.

The retinocollicular projection in the marsupial mammal the wallaby Macropus eugenii, has been investigated anatomically to determine the order in the developing projection and electrophysiologically to determine the time of onset of synaptic transmission by recording evoked potentials in the colliculus in response to stimulation of the optic nerve. There are two clear stages: a protracted period when retinal axons grow into the colliculus in coarse retinotopic order with no recordable electrical activity followed by the formation of terminal zones in retinotopically correct positions, the loss of more widely distributed axons and the onset of evoked potentials. The two stages are not seen in non-mammalian vertebrates where the projection is functional from the beginning.

Marsupial retinocollicular system shows differential expression of messenger RNA encoding EphA receptors and their ligands during development

The protracted development of the wallaby (Macropus eugenii) has allowed study of messenger RNAs encoding Eph receptors EphA3 and EphA7 and ligands ephrin‐A2 and ‐A5 in the retina and superior colliculus at intervals throughout the development of the retinocollicular projection: from birth, before retinal innervation, to postnatal day 95, when the projection is mature. Reverse transcription‐polymerase chain reaction showed messenger RNAs for both receptors and ligands were expressed at all ages. EphA7 was expressed more highly in the rostral superior colliculus. Ephrin‐A2 and ‐A5 were expressed more highly in the caudal colliculus. EphA3 was expressed in a complementary manner, more highly in temporal than in nasal retina. There are higher levels of expression of the ligands when the projection is only coarsely topographically organised. This suggests a role for them and their receptor EphA3 in this stage, by repulsive interactions which restrict temporal axons to rostral superior colliculus. This is the first account in a marsupial mammal of the appearance of this molecular family, substantiating its ubiquitous role in topographically organised neuronal connections. Nevertheless, expression is not the same as in the mouse, suggesting differences in the details of topographic coding between species. J. Neurosci. Res. 57:244–254, 1999.

The effect of striatal lesions in the chick on haloperidol-potentiated tonic immobility

The potentiating effects of haloperidol on tonic immobility in chickens were reduced in birds given bilateral injections of kainic acid into the paleostriatum. Aspiration of tissue above the lamina medullaris dorsalis, which includes the neostriatum and hyperstriatum, had no significant effect on haloperidol-potentiated tonic immobility. The results support the suggestion that the paleostriatum of birds is homologous to the basal ganglia of mammals.

Innervation pattern of muscles of one-legged Xenopus laevis supplied by motoneurons from both sides of the spinal cord

In Xenopus tadpoles one limb bud was removed before innervation and motoneurons from both sides of the spinal cord were induced to innervate the remaining limb. When examined after metamorphosis the motor innervation of the limb had the following characteristics. In agreement with previous findings a large proportion of contralateral motoneurons survived (51-82% of the ipsilateral numbers) and sent axons to the limb. By acetylcholinesterase staining and intracellular recording from muscle fibers of the response to electrical stimulation of the two limb innervations, the neuromuscular junctions from contralateral motoneurons were indistinguishable from those from the ipsilateral side in their morphology, spacing along the fiber, and physiological properties. Many single muscle fibers shared innervation from both sides of the cord by symmetrically placed spinal nerves. By the same techniques junctions in one-legged frogs were morphologically indistinguishable from those in normal frogs, but the quantal content of transmitter release was increased by up to 63%. Recording twitch and tetanic tensions from individual motor units from the gastrocnemius muscle showed that the one-legged animals had many more and smaller motor units than do normal frogs. We confirm that the hind-limb musculature has the ability, normally unexpressed, to sustain, through the period of normal developmental cell death, up to twice the usual number of motoneurons. In maturity, motoneurons accommodate themselves to the limb muscles by making fewer than the normal number of synapses. The above suggests that developmental motoneuron death is not primarily a mechanism for adjusting the number of motoneurons to the size of the peripheral musculature and is likely to be related to mechanisms for securing specific neuromuscular connections.

Retinotectal reorganization in goldfish—I. Effects of season, lighting conditions and size of fish

Abstract If the caudal half of the goldfish tectum is removed reorganization may take place so that the representation of the whole visual field is compressed on to the remaining half tectum. We have found that such reorganization only takes place during summer. Fish operated on in the autumn and mapped during winter do not undergo compression. Taking this seasonal effect into account and using fish larger than 6.0cm in body length, we are now able to repeat the previously reported effect of exposure to constant light in preventing compression. In a proportion of smaller fish exposure to constant light can induce compression during winter. Electron microscopy shows that failure of compression of the retinotectal projection in large fish, whether due to season or lighting conditions, is not because of lack of axonal growth. We suggest that a common factor, perhaps hormonal, prevents the development or maturation of synaptic connections in both situations.