Bimodal Neurons Research Articles

Responses of a bimodal neuron (chemo- and vibration-sensitive) on the walking legs of the crayfish

On the walking legs of crayfish,Austropotamobius torrentium, arranged in tufts over the chela, are large (smooth) setae. Electrophysiological recordings have demonstrated the presence within them of bimodal neurons with highly sensitive and specific responses to vibration and to chemical stimuli. Vibration at frequencies up to ca 45 Hz elicited a single, synchronized action potential per pulse; at higher frequencies many pulses failed to elicit a potential. The chemical stimuli found to be effective were nicotinamide and related substances (KM 5×10−5 mol/l), and again the saturation frequency was about 45 imp/s. There were no discernible differences in amplitude, time course or duration between the action potentials elicited by chemical stimuli and those elicited by vibration. Particularly strong evidence that these neurons are genuinely bimodal is the finding that chemical stimuli can modulate the sensitivity to vibration and that vibration alters the threshold and magnitude of the response to chemical stimuli.

Integration of visual and auditory information in bimodal neurones in the guinea-pig superior colliculus.

We have investigated the responses of neurones in the guinea-pig superior colliculus to combinations of visual and auditory stimuli. When these stimuli were presented separately, some of these neurones responded only to one modality, others to both and a few neurones reliably to neither. To bimodal stimulation, many of these neurones exhibited some form of cross-modality interaction, the degree and nature of which depended on the relative timing and location of the two stimuli. Facilitatory and inhibitory interactions were observed and, occasionally, both effects were found in the same neurone at different inter-stimulus intervals. Neurones whose responses to visual stimuli were enhanced by an auditory stimulus were found in the superficial layers. Although visual-enhanced and visual-depressed auditory neurones were found throughout the deep layers, the majority of them were recorded in the stratum griseum profundum. Neurones that responded to both visual and auditory stimuli presented separately and gave enhanced or depressed responses to bimodal stimulation were found throughout the deep layers, but were concentrated in the stratum griseum intermediale and extended into the stratum opticum.

Visual responses in the postarcuate cortex (area 6) of the monkey that are independent of eye position

The visual responses of postarcuate neurons have been studied in alert behaving monkeys (Macaca nemestrina). In particular, the effect of eye position on the location of visual responses in respect to the body has been examined. It was found that a large percentage of bimodal (visual and somatosensory) neurons have visual receptive fields that are independent of eye position. The location of the visual receptive field does not change when the eyes move, but remains in register with the tactile receptive field (soma-related visually responsive neurons).

The orbitofrontal cortex: neuronal activity in the behaving monkey.

Single unit recording of neurons in the orbitofrontal cortex of the alert rhesus monkey was used to investigate responses to sensory stimulation. 32.4% of the neurons had visual responses that had typical latencies of 100-200 ms, and 9.4% responded to gustatory inputs. Most neurons were selective, in that they responded consistently to some stimuli such as foods or aversive objects, but not to others. In a number of cases the neurons responded selectively to particular foods or aversive stimuli. However, this high selectivity could not be explained by simple sensory features of the stimulus, since the responses of some neurons could be readily reversed if the meaning of the stimulus (i.e. whether it was food or aversive) was changed, even though its physical appearance remained identical. Further, some bimodal neurons received convergent visual and gustatory inputs, with matching selectivity for the same stimulus in both modalities, again suggesting that an explanation in terms of simple sensory features is inadequate. Neurons were also studied during the performance of tasks known to be disrupted by orbitofrontal lesions, including a go/no go visual discrimination task and its reversal. 8.6% of neurons had differential responses to the two discriminative stimuli in the task, one of which indicated that reward was available and the other saline. Reversing the meaning of the two stimuli showed that whereas some differential units were closely linked to the sensory features of the stimuli, and some to their behavioural significance, others were conditional, in that they would only respond if a particular stimulus was present, and if it was the one being currently rewarded. Other neurons had activity related to the outcome of the animal's response, with some indicating that reinforcement had been received and others, that an error had been made and that a reversal was required. Thus, neurons in the orbitofrontal cortex possess highly coded information about which stimuli are present, as well as information about the consequences of the animal's own responses. It is suggested that together they may constitute a neuronal mechanism for determining whether particular visual stimuli continue to be associated with reinforcement, as well as providing for the modification of the animal's behavioural responses to such stimuli when those responses are no longer appropriate.

Integration of visual and infrared information in bimodal neurons in the rattlesnake optic tectum.

Bimodal neurons in the rattlesnake tectum, which receive sensory input from the retina and from the infrared-sensing pit organ, exhibit novel, highly nonlinear cross-modality interactions. Some units respond only to simultaneous bimodal stimulation. Others respond to only one of the two modalities, but show greatly enhanced or depressed responses when stimulated simultaneously in the second modality. These cross-modality interactions may play an important role in recognizing and orienting toward biologically important objects.

Afferent properties of periarcuate neurons in macaque monkeys. I. Somatosensory responses

The afferent properties of single neurons of the periarcuate cortex have been studied in the macaque monkey. Most of the recorded neurons responded to stimuli in one or two sensory modalities and, accordingly, they were classified as somatosensory, visual or bimodal (visual and somatosensory) neurons. Visual neurons were located rostral to the arcuate sulcus, whereas the somatosensory and the bimodal neurons were found predominantly caudal to this sulcus. Somatosensory neurons (n = 102) and bimodal neurons (n = 69) had identical somatic afferent properties. They were subdivided into ‘tactile’ neurons, ‘joint’ neurons and ‘tactile and joint’ neurons. ‘Tactile’ neurons (70%) had their receptive fields formed either by one or by two or more spatially separated responding areas. The parts of the body most represented were the hands and the mouth. ‘Joint’ neurons (10%) were activated by the rotation of one or, more often, of two or more articulations. The movement of the hand towards the mouth was the most frequently represented movement. ‘Tactile and joint’ neurons (20%) responded to both tactile and joint stimulation having receptive field locations and properties like those of the other two classes of neurons. Some ‘joint’ and ‘tactile and joint’ neurons had summing properties, i.e. their response to tactile or joint stimulation was conditional upon a simultaneous stimulation of another articulation. The data are interpreted as evidence in favor of the existence of an area in the agranular cortex that organizes the mouth and the hand to mouth movements.

Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses

The visual responses of single neurons of the periarcuate cortex have been studied in the macaque monkey. Two sets of neurons responding to visual stimuli have been found. The first set, located rostral to the arcuate sulcus, was formed by units that could be activated by stimuli presented far from the animal. These neurons had large receptive fields and were neither orientation nor direction selective. The second set, found predominantly caudal to the arcuate sulcus, was formed by units that were maximally or even exclusively activated by stimuli presented in the space immediately around the animal. These neurons were bimodal, responding also to somatosensory stimuli. According to the location of their visual responding regions the bimodal neurons were subdivided into pericutaneous (54%) and distant peripersonal neurons (46%). The former responded best to stimuli presented a few centimeters from the skin, the latter to stimuli within the animal's reaching distance. The visual responding regions were spatially related to the tactile fields. It is argued that neurons with a receptive field consisting of several responding areas, some in one sensory modality, some in another, have a praxic function and that they are involved in organizing sequences of movements.

Anatomical and physiological localization of visual and infrared cell layers in tectum of pit vipers.

Visual and infrared cell layers were identified in the tectum of the pit vipers Crotalus viridis and Sistrurus melitus. Histologic reconstructions of 48 lesions utilizing the Prussian Blue technique were correlated with micrometer depth readings for 251 visual, infrared and bimodal single unit recordings. The visual cell layer extends caudally from approximately the level of the habenula to the rostral border of the posterior corpora quadrigemina. Neurons responding to visual stimulation are generally contained within zones 7b-13, i.e., the superficial 600--700 micrometer of the optic tectum (stratum fibrosum et griseum superficiale and the superficial sublayer of stratum griesum centrale). The infrared cell group is found in layer 7 (a and b; stratum griseum centrale) throughout the optic tectum. Eighty percent of the infrared neurons are found within 500--1,200 micrometer of the surface. In layer 7b the visual and infrared cell groups are mixed; bimodal neurons that respond to a combination of visual and infrared input are located predominantly in this sublamina. The lamination pattern for visual and nonvisual cell groups in the rattlesnake tectum appears to more closely resemble the colubrid tectum and mammalian superior colliculus than the tecta of other reptiles.

Merging of modalities in the optic tectum: infrared and visual integration in rattlesnakes.

The optic tectum of pit vipers (Crotalinae) contains a layer of infrared-sensitive neurons subjacent to the visual layer; these indirectly receive input from the facial pit organs. They respond transiently to the appearance or motion of warm objects within their 25 degrees to 70 degrees excitatory receptive fields (some have inhibitory regions) and presumably allow the snake to orient or strike toward prey. The infrared and visual spatiotopic tectal maps have similar but not identical axes; the infrared magnification is greater than that for vision. Bimodal neurons have receptive fields for each modality that reflect the disparity of the two maps. This finding suggests that (i) during development the infrared and visual fibers spread out independently to fill available tectal sites and (ii) bimodal neurons form local connections without regard to establishing spatial correspondence between the two modalities.

Vestibular responses in the Rhesus monkey ventroposterior thalamus. II. Vestibulo-proprioceptive convergence at thalamic neurons

The vestibular thalamic relay in the Rhesus ventrobasal complex, identified in a previous field potential study (part I, Deecke et al., 1974), has now been investigated with neuronal recordings in the thalamus in order to clarify its functional role. In part I, short latency responses (2.5 msec) were found in the corner between VPL, VPM and VPI nuclei, largely including dorsal portions of the VPI nucleus. Field potentials of somewhat longer latency (4-5 msec) were recorded in VPL and in other thalamic nuclei, including the posterior nuclear group. Neuronal responses were recorded in thalamic nuclei of awake flaxedilized Rhesus monkeys. Cells not responding to vestibular stimulation (round window polarisation of either labyrinth) were ignored. The great majority (80%) of those neurons responding to labyrinth polarisation showed convergence with deep somatic (proprioceptive) input from joints and muscles of vertebral column and limbs. 60% of these bimodal neurons responded to movement of cervical joints. Very few vestibularly responsive cells received cutaneous (6.6%), non-optokinetic visual or auditory (2.6% each) input. Proprioceptive fields tended to be large, frequently involving more than one joint, and could be even bilateral. For a few cells the pattern of vestibulo-proprioceptive convergence could be fitted to a coordinated body position that might occur during normal locomotion. 78% of the cells responded to polarisation of both labyrinths, indicating strong bilateral projection.

Interaction between impulses evoked by stimuli of different modalities in neurons of the parietal associative cortex.

In acute experiments on cats anesthetized with chloralose and nembutal interaction between visual, auditory, and electrodermal stimuli in neurons of the parietal association cortex was studied. Two types of interaction were found; the first characterized by inhibition or by inhibition followed by facilitation of the response to the test stimulus, the second by facilitation or by facilitation followed by inhibition of spontaneous impulses. Interaction between stimuli of different modalities was shown to depend on the properties of the neuron. In polysensory neurons ability to interact was much higher than in bimodal or monomodal neurons.

Respones of trigeminal ganglion and brain stem neurones in the cat to mechanical and thermal stimulation of the face

Microelectrode penetrations were made in the trigeminal ganglion and brain stem nuclei to characterize the responses of single neurones to mechanical and thermal stimulation of the hairy skin of the face of the unanaesthetized cat. The mechanoreceptive fields of primary neurones innervating the hairy skin of the face were associated with 3 hair follicle types. Receptive fields involving single vibrissae were the most common. Both slowly and rapidly adapting units innervated each follicle type and a preliminary survey of peripheral conduction velocity indicated that the neurones were associated with myelinated nerve fibres. The mechanical response properties of brain stem neurones in nuclei oralis and caudalis of the unanaesthetized cat were similar to those noted in previous investigations of decerebrate or anaesthetized animals. The receptive field areas of brain stem neurones were considerably larger than those of primary neurones. Moreover, receptive fields in the perioral region of the face were significantly smaller than receptive fields in posterior facial areas. Many of these mechanosensitive neurones were also responsive to thermal changes in their receptive field. There was no evidence of specific thermoreceptive units innervating facial hairy skin in either the trigeminal ganglion or brain stem nuclei of the unanaesthetized cat. This contrasts with previous findings of specific thermoreceptors in intraoral and peri-nasal regions. Most of the bimodal neurones showed marked sensitivity to even small temperature changes. The common response was an increased discharge to cooling and a depression of discharge on warming. A few units showed some sensitivity to constant temperatures. The response properties of bimodal neurones in nuclei oralis and caudalis could be completely accounted for by an input from primary neurones sensitive to mechanical as well as thermal stimulation.

Responses of cortical neurons to viscero-somatic stimulation

Responses of cortical neurons in the posterior sigmoid gyrus of cats anesthetized with chloralose to electrical stimulation of somatic and visceral nerves were recorded. Bimodal viscero-somatic neurons are predominant in this part of the cortex and some of them also respond to light. Besides the polysensory modally-specific neurons it was also possible to distinguish a group of modally nonspecific cells (27%), whose responses to different stimuli did not differ statistically from each other. Simultaneous stimulation of visceral and somatic nerves led to facilitation of activity of the long-latency neurons; this was reflected in a decrease of 10 msec in the latent period of the response and an increase in the number of spikes per discharge.