Primate-like retinotectal decussation in an echolocating megabat, Rousettus aegyptiacus.

The current study was designed to reveal the retinotectal pathway in the brain of the echolocating megabat Rousettus aegyptiacus. The retinotectal pathway of other species of megabats shows the primate-like pattern of decussation in the retina; however, it has been reported that the echolocating Rousettus did not share this feature. To test this prior result we injected fluorescent dextran tract tracers into the right (fluororuby) and left (fluoroemerald) superior colliculi of three adult Rousettus. After a 2-week survival period the animals were killed, fixed via transcardial perfusion, and the retinas whole mounted and examined under fluorescent excitation to reveal the pattern of retrograde transport. Red and green labeled retinotectal ganglion cells were found in side-by-side patches on either side of a vertical decussation line in the temporal retina of all six retinas. The Rousettus examined thus exhibited the same pattern of retinal decussation as reported previously for other megabats and primates, but unlike that seen in other mammals. The current result indicates that the prior study appears to have suffered technical problems leading to an incorrect conclusion. The results of our study indicate that, as may be expected, all megabats share the derived retinotectal pathway once thought to be the exclusive domain of primates. The current study provides additional support for the diphyletic origin of the Chiroptera and aligns the megabats phylogenetically as a sister group to primates.

Slow binocular rivalry in bipolar disorder.

BACKGROUND: The rate of binocular rivalry has been reported to be slower in subjects with bipolar disorder than in controls when tested with drifting, vertical and horizontal gratings of high spatial frequency. METHOD: Here we assess the rate of binocular rivalry with stationary, vertical and horizontal gratings of low spatial frequency in 30 subjects with bipolar disorder, 30 age- and sex-matched controls, 18 subjects with schizophrenia and 18 subjects with major depression. Along with rivalry rate, the predominance of each of the rivaling images was assessed, as was the distribution of normalized rivalry intervals. RESULTS: The bipolar group demonstrated significantly slower rivalry than the control, schizophrenia and major depression groups. The schizophrenia and major depression groups did not differ significantly from the control group. Predominance values did not differ according to diagnosis and the distribution of normalized rivalry intervals was well described by a gamma function in all groups. CONCLUSIONS: The results provide further evidence that binocular rivalry is slow in bipolar disorder and demonstrate that rivalry predominance and the distribution of normalized rivalry intervals are not abnormal in bipolar disorder. It is also shown by comparison with previous work, that high strength stimuli more effectively distinguish bipolar from control subjects than low strength stimuli. The data on schizophrenia and major depression suggest the need for large-scale specificity trials. Further study is also required to assess genetic and pathophysiological factors as well as the potential effects of state, medication, and clinical and biological subtypes.

The distribution and morphological characteristics of catecholaminergic cells in the brain of monotremes as revealed by tyrosine hydroxylase immunohistochemistry.

The present study describes the distribution and cellular morphology of catecholaminergic neurons in the CNS of two species of monotreme, the platypus (Ornithorhynchus anatinus) and the short-beaked echidna (Tachyglossus aculeatus). Tyrosine hydroxylase immunohistochemistry was used to visualize these neurons. The standard A1-A17, C1-C3 nomenclature was used for expediency, but the neuroanatomical names of the various nuclei have also been given. Monotremes exhibit catecholaminergic neurons in the diencephalon (A11, A12, A13, A14, A15), midbrain (A8, A9, A10), rostral rhombencephalon (A5, A6, A7), and medulla (A1, A2, C1, C2). The subdivisions of these neurons are in general agreement with those of other mammals, and indeed other amniotes. Apart from minor differences, those being a lack of A4, A3, and C3 groups, the catecholaminergic system of monotremes is very similar to that of other mammals. Catecholaminergic neurons outside these nuclei, such as those reported for other mammals, were not numerous with occasional cells observed in the striatum. It seems unlikely that differences in the sleep phenomenology of monotremes, as compared to other mammals, can be explained by these differences. The similarity of this system across mammalian and amniote species underlines the evolutionary conservatism of the catecholaminergic system.

The distribution and morphological characteristics of serotonergic cells in the brain of monotremes.

The distribution and cellular morphology of serotonergic neurons in the brain of two species of monotremes are described. Three clusters of serotonergic neurons were found: a hypothalamic cluster, a cluster in the rostral brainstem and a cluster in the caudal brainstem. Those in the hypothalamus consisted of two groups, the periventricular hypothalamic organ and the infundibular recess, that were intimately associated with the ependymal wall of the third ventricle. Within the rostral brainstem cluster, three distinct divisions were found: the dorsal raphe nucleus (with four subdivisions), the median raphe nucleus and the cells of the supralemniscal region. The dorsal raphe was within and adjacent to the periaqueductal gray matter, the median raphe was associated with the midline ventral to the dorsal raphe, and the cells of the supralemniscal region were in the tegmentum lateral to the median raphe and ventral to the dorsal raphe. The caudal cluster consisted of three divisions: the raphe obscurus nucleus, the raphe pallidus nucleus and the raphe magnus nucleus. The raphe obscurus nucleus was associated with the dorsal midline at the caudal-most part of the medulla oblongata. The raphe pallidus nucleus was found at the ventral midline of the medulla around the inferior olive. Raphe magnus was associated with the midline of the medulla and was found rostral to both the raphe obscurus and raphe pallidus. The results of our study are compared in an evolutionary context with those reported for other mammals and reptiles.

The distribution and morphological characteristics of cholinergic cells in the brain of monotremes as revealed by ChAT immunohistochemistry.

The present study employs choline acetyltransferase (ChAT) immunohistochemistry to identify the cholinergic neuronal population in the central nervous system of the monotremes. Two of the three extant species of monotreme were studied: the platypus (Ornithorhynchus anatinus) and the short-beaked echidna (Tachyglossus aculeatus). The distribution of cholinergic cells in the brain of these two species was virtually identical. Distinct groups of cholinergic cells were observed in the striatum, basal forebrain, habenula, pontomesencephalon, cranial nerve motor nuclei, and spinal cord. In contrast to other tetrapods studied with this technique, we failed to find evidence for cholinergic cells in the hypothalamus, the parabigeminal nucleus (or nucleus isthmus), or the cerebral cortex. The lack of hypothalamic cholinergic neurons creates a hiatus in the continuous antero-posterior aggregation of cholinergic neurons seen in other tetrapods. This hiatus might be functionally related to the phenomenology of monotreme sleep and to the ontogeny of sleep in mammals, as juvenile placental mammals exhibit a similar combination of sleep elements to that found in adult monotremes.

Spontaneous and stimulus-evoked intrinsic optical signals in primary auditory cortex of the cat.

Spontaneous and tone-evoked changes in light reflectance were recorded from primary auditory cortex (A1) of anesthetized cats (barbiturate induction, ketamine maintenance). Spontaneous 0.1-Hz oscillations of reflectance of 540- and 690-nm light were recorded in quiet. Stimulation with tone pips evoked localized reflectance decreases at 540 nm in 3/10 cats. The distribution of patches "activated" by tones of different frequencies reflected the known tonotopic organization of auditory cortex. Stimulus-evoked reflectance changes at 690 nm were observed in 9/10 cats but lacked stimulus-dependent topography. In two experiments, stimulus-evoked optical signals at 540 nm were compared with multiunit responses to the same stimuli recorded at multiple sites. A significant correlation (P < 0.05) between magnitude of reflectance decrease and multiunit response strength was evident in only one of five stimulus conditions in each experiment. There was no significant correlation when data were pooled across all stimulus conditions in either experiment. In one experiment, the spatial distribution of activated patches, evident in records of spontaneous activity at 540 nm, was similar to that of patches activated by tonal stimuli. These results suggest that local cerebral blood volume changes reflect the gross tonotopic organization of A1 but are not restricted to the sites of spiking neurons.

Colour vision in billfish.

Members of the billfish family are highly visual predatory teleosts inhabiting the open ocean. Little is known about their visual abilities in detail, but past studies have indicated that these fishes were likely to be monochromats. This study, however, presents evidence of two anatomically distinct cone types in billfish. The cells are arranged in a regular mosaic pattern of single and twin cones as in many fishes, and this arrangement suggests that the different cone types also show different spectral sensitivity, which is the basis for colour vision. First measurements using microspectrophotometry (MSP) revealed a peak absorption of the rod pigment at 484 nm, indicating that MSP, despite technical difficulties, will be a decisive tool in proving colour vision in these offshore fishes. When hunting, billfish such as the sailfish flash bright blue bars on their sides. This colour reflects largely in ultraviolet (UV) light at 350 nm as revealed by spectrophotometric measurements. Billfish lenses block light of wavelengths below 400 nm, presumably rendering the animal blind to the UV component of its own body colour. Interestingly, at least two prey species of billfish have lenses transmitting light in the UV waveband and are therefore likely to perceive a large fraction of the UV peak found in the blue bar of the sailfish. The possible biological significance of this finding is discussed.

Prey capture and accommodation in the sandlance, Limnichthyes fasciatus (Creediidae; Teleostei).

The eyes of the sandlance, Limnichthyes fas ciatus (Creediidae, Teleostei) move independently and possess a refractive cornea, a convexiclivate fovea and a non-spherical lens giving rise to a wide separation of the nodal point from the axis of rotation of the eye much like that of a chameleon. To investigate this apparent convergence of the visual optics in these phylogenetically disparate species, we examine feeding behaviour and accommodation in the sandlance with special reference to the possibility that sandlances use accommodation as a depth cue to judge strike length. Frame-by-frame analysis of over 2000 strikes show a 100% success rate. Explosive strikes are completed in 50 ms over prey distances of four body lengths. Close-up video confirms that successful strikes can be initiated monocularly (both normally and after monocular occlusion) showing that binocular cues are not necessary to judge the length of a strike. Additional means of judging prey distance may also be derived from partallax information generated by rotation of the eye as suggested for chameleons. Using photorefraction on anaesthetised sandlances, accommodative changes were induced with acetylcholine and found to range between 120 D and 180 D at a speed of 600-720 D s(-1). The large range of accommodation (25% of the total power) is also thought to be mediated by corneal accommodation where the contraction of a unique cornealis muscle acts to change the corneal curvatures.

Interhemispheric switching mediates perceptual rivalry.

BACKGROUND: Binocular rivalry refers to the alternating perceptual states that occur when the images seen by the two eyes are too different to be fused into a single percept. Logothetis and colleagues have challenged suggestions that this phenomenon occurs early in the visual pathway. They have shown that, in alert monkeys, neurons in the primary visual cortex continue to respond to their preferred stimulus despite the monkey reporting its absence. Moreover, they found that neural activity higher in the visual pathway is highly correlated with the monkey's reported percept. These and other findings suggest that the neural substrate of binocular rivalry must involve high levels, perhaps the same levels involved in reversible figure alternations. RESULTS: We present evidence that activation or disruption of a single hemisphere in human subjects affects the perceptual alternations of binocular rivalry. Unilateral caloric vestibular stimulation changed the ratio of time spent in each competing perceptual state. Transcranial magnetic stimulation applied to one hemisphere disrupted normal perceptual alternations when the stimulation was timed to occur at one phase of the perceptual switch, but not at the other. Furthermore, activation of a single hemisphere by caloric stimulation affected the perceptual alternations of a reversible figure, the Necker cube. CONCLUSIONS: Our findings suggest that interhemispheric switching mediates perceptual rivalry. Thus, competition for awareness in both binocular rivalry and reversible figures occurs between, rather than within, each hemisphere. This interhemispheric switch hypothesis has implications for understanding the neural mechanisms of conscious experience and also has clinical relevance as the rate of both types of perceptual rivalry is slow in bipolar disorder (manic depression).

Sleep in the platypus.

We have conducted the first study of sleep in the platypus Ornithorhynchus anatinus. Periods of quiet sleep, characterized by raised arousal thresholds, elevated electroencephalogram amplitude and motor and autonomic quiescence, occupied 6-8 h/day. The platypus also had rapid eye movement sleep as defined by atonia with rapid eye movements, twitching and the electrocardiogram pattern of rapid eye movement. However, this state occurred while the electroencephalogram was moderate or high in voltage, as in non-rapid eye movement sleep in adult and marsupial mammals. This suggests that the low-voltage electroencephalogram is a more recently evolved feature of mammalian rapid eye movement sleep. Rapid eye movement sleep occupied 5.8-8 h/day in the platypus, more than in any other animal. Our findings indicate that rapid eye movement sleep may have been present in large amounts in the first mammals and suggest that it may have evolved in pre-mammalian reptiles.

Convergence of specialised behaviour, eye movements and visual optics in the sandlance (Teleostei) and the chameleon (Reptilia)

Chameleons have a number of unusual, highly specialised visual features, including telescopic visual optics with a reduced lens power, wide separation of the eye's nodal point from the axis of rotation, a deep-pit fovea, rapid pre-calculated strikes for prey based on monocular depth judgements (including focus), and a complex pattern of partially independent alternating eye movements. The same set of features has been acquired independently by a teleost, the sandlance Limnichthyes fasciatus. Despite its underwater lifestyle, this fish displays visual behaviour and rapid strikes for prey that are remarkably similar to those of the chameleon [1]. In a direct comparison of the two species, we have revealed other, previously unsuspected, similarities, such as corneal accommodation, which was unknown in teleosts, as well as bringing together, for the first time, data collected from both species. The sandlance is the only teleost, among thousands studied, that has corneal refraction, corneal accommodation and reduced lens power, as well as sharing the other specialised optical features seen in chameleons. The independent eye movement pattern in the sandlance is also unusual and similar to that of the chameleon. The selection pressures that have produced this remarkable example of convergence may relate to common visual constraints in the life styles of these two phylogenetically disparate species.

Electroreception in monotremes.

I will briefly review the history of the bill sense of the platypus, a sophisticated combination of electroreception and mechanoreception that coordinates information about aquatic prey provided from the bill skin mechanoreceptors and electroreceptors, and provide an evolutionary account of electroreception in the three extant species of monotreme (and what can be inferred of their ancestors). Electroreception in monotremes is compared and contrasted with the extensive body of work on electric fish, and an account of the central processing of mechanoreceptive and electroreceptive input in the somatosensory neocortex of the platypus, where sophisticated calculations seem to enable a complete three-dimensional fix on prey, is given.

Morphology of pyramidal neurones in cytochrome oxidase modules of the S-I bill representation of the platypus.

The primary somatosensory cortex of the platypus (Ornithorhynchus anatinus) is characterized by a distinct array of functionally specific cytochrome oxidase (CO) modules, forming alternate CO-rich and CO-poor bands. In the current study, we undertook to establish whether the cellular morphology of layer V pyramidal neurones reflects this modular organization. To this end, we injected neurones with Lucifer Yellow in 250 microm thick, flat-mounted cortical slices and processed the tissue to reveal a light-stable reaction product. By aligning blood vessels in serial sections in which we injected individual neurones with sections processed for CO, we were able to establish the exact location of injected cells with respect to the pattern of CO bands. Pyramidal neurones in the CO-poor bands (which are responsive to both mechano- and electroreceptive stimuli) had basal dendritic fields that were larger than those in the CO-rich bands. The large basal dendritic fields of layer V pyramidal neurones in the CO-poor bands may allow for integration of a greater number of more diverse inputs, thus allowing for averaging of stimuli to improve the signal-to-noise ratio or enhance spatial discrimination of peripheral stimuli. In some instances, neurones located within approximately 100 microm of the boundaries of the CO bands had dendritic fields that appeared to conform to the CO bands, the dendrites preferentially arborizing within a single band and avoiding the neighbouring band. However, the bias was not absolute, as we observed many examples of cells with dendrites that crossed the boundary between bands. Furthermore, many cells had dendrites that showed distinct dendritic bias that bore no obvious relationship to the CO boundaries.

The development of the external features of the platypus (Ornithorhynchus anatinus).

The present study describes the post-hatching development of the external features of the platypus. Specimens range in age from the day of hatching through to 6 months old, and provide the first comprehensive view of the developmental sequence of these features. Various features, those specific to the platypus, those specific to monotremes and those shared with marsupials and eutherians, are described. Features specific to the platypus, including the bill and webbing of the forefeet, are seen to develop precociously. Many features show similarities to marsupials, although marsupials show differential development both in timing and in morphology. The developmental progression is related to the age, in days, although the exact age of the specimens is unclear, and relies on ages given to the specimens at the time of collection, sometimes as long as 70 years ago. Despite this, the progression of development of these features suggests that the ageing given is relatively accurate.

Distribution and putative function of autonomic nerve fibres in the bill skin of the platypus (Ornithorhynchus anatinus).

The electroreceptors located in the bill skin of the platypus are modified secretory glands. The electroreceptive nerve terminals form bare endings in close proximity to the duct of these glands. In this study, we describe the autonomic innervation of the glands and a separate specialized autonomic innervation of the epidermal portion of the glandular duct. A range of immunohistochemical labels showed that the gland cells of the electroreceptors have a non-noradrenergic (putative parasympathetic) innervation. Phalloidin labelling revealed a 'sphincter' of epidermal luminal cells that labelled strongly for actin. These actin-dense keratinocytes were seen to have a noradrenergic (putative sympathetic) innervation. Fine-diameter sensory fibres containing substance P (presumably C-fibre thermoreceptors or polymodal nociceptors) were observed to terminate in the superficial epidermis surrounding the pore of the gland. When the bill of the platypus is dry these pores were closed. However, when room temperature water was washed over the bill, the pores opened. It is proposed that this autonomic and sensory innervation, along with the actin sphincter, mediates the opening and closing of the pores. By doing this, the platypus prevents the desiccation of the bare electrosensory nerve terminals when it is out of the water, and it may also be a way to regulate the impedance of the internal electrical circuit presented to the water at the pores.

Monotremes and the evolution of rapid eye movement sleep.

Early studies of the echidna led to the conclusion that this monotreme did not have rapid eye movement (REM) sleep. Because the monotremes had diverged from the placental and marsupial lines very early in mammalian evolution, this finding was used to support the hypothesis that REM sleep evolved after the start of the mammalian line. The current paper summarizes our recent work on sleep in the echidna and platypus and leads to a very different interpretation. By using neuronal recording from mesopontine regions in the echidna, we found that despite the presence of a high-voltage cortical electroencephalogram (EEG), brainstem units fire in irregular bursts intermediate in intensity between the regular non-REM sleep pattern and the highly irregular REM sleep pattern seen in placentals. Thus the echidna displays brainstem activation during sleep with high-voltage cortical EEG. This work encouraged us to do the first study of sleep, to our knowledge, in the platypus. In the platypus we saw sleep with vigorous rapid eye, bill and head twitching, identical in behaviour to that which defines REM sleep in placental mammals. Recording of the EEG in the platypus during natural sleep and waking states revealed that it had moderate and high-voltage cortical EEGs during this REM sleep state. The platypus not only has REM sleep, but it had more of it than any other animal. The lack of EEG voltage reduction during REM sleep in the platypus, and during the REM sleep-like state of the echidna, has some similarity to the sleep seen in neonatal sleep in placentals. The very high amounts of REM sleep seen in the platypus also fit with the increased REM sleep duration seen in altricial mammals. Our findings suggest that REM sleep originated earlier in mammalian evolution than had previously been thought and is consistent with the hypothesis that REM sleep, or a precursor state with aspects of REM sleep, may have had its origin in reptilian species.