F.M. de Monasterio

Functional properties of ganglion cells of the rhesus monkey retina.

Three general classes of cells were identified in a sample of 460 cells recorded from all areas of the retina subserving the central 40 degrees of vision in the rhesus monkey. 2. One class (colour‐opponent) had sustained colour‐opponent responses and concentrically organized receptive fields, in which usually one cone mechanism mediated the centre response and one or two different cone mechanisms mediated the antagonistic surround. A few cells of this class had non‐concentric (co‐extensive) receptive field organization. 3. A second class (broad‐band) had transient responses and concentrically organized receptive fields, in which usually two cone mechanisms mediated the centre response. In most cells, the surround had the same spectral sensitivity as the centre and the cells had non‐colour opponent responses. In other cells, the surround had a spectral sensitivity different to that of the centre and the cells had colour‐opponent responses. 4. The third class (non‐concentric) did not have concentrically organized receptive fields. One group of cells had extremely phasic on‐, off‐ or on‐off responses and no spontaneous activity, another group had characteristically regular spontaneous activity and was responsive only to moving stimuli. 5. Cells of the colour‐opponent class with concentric receptive fields had the smallest centre‐sizes, which did not vary markedly from cell to cell (mean 15 mum); cells of the non‐concentric class with phasic responses had the largest centre‐sizes, which varied from cell to cell. 6. Colour‐opponent cells comprised the highest proportion of cells near the foveola; broad‐band cells comprised the highest proportion in the more peripheral areas of the retina; non‐concentric cells were equally represented in all areas.

Trichromatic colour opponency in ganglion cells of the rhesus monkey retina.

Two hundred and eleven colour‐opponent ganglion cells were studied in the central 10 degrees of the retina of the rhesus monkey, to determine the inputs which they were receiving from different cone mechanisms. Spectral‐sensitivity measurements in the presence of neutral and coloured back‐grounds showed that 24% of these cells appeared to receive input from all three cone mechanisms. 2. In 3% of the cells, the red‐sensitive cone mechanism opposed the blue‐ and green‐sensitive ones. In 18% of the cells, the blue‐sensitive cone mechanism opposed the green‐ and red‐sensitive ones. In 3% of the cells, the green‐sensitive cone mechanism opposed the blue‐ and red‐sensitive ones. 3. In 12% of the cells receiving opponent green‐ and red‐sensitive cone inputs, responses from the beta‐band of the red‐sensitive cone mechanism could be detected and distinguished from blue‐sensitive cone input. 4. All cells receiving blue‐sensitive cone input appeared to be trichromatic. The retinal distribution of cells with trichromatic input and that of cells with beta‐band responses seemed to parallel the availability of blue‐sensitive cones in the retinal area being considered. 5. The results indicate that trichromatic interactions in the macaque visual system begin in the retina.

Asymmetry of on- and off-pathways of blue-sensitive cones of the retina of macaques.

Abstract Macaque retinal ganglion cells whose receptive-field center recieves input from blue-sensitive cones show an overt asymmetry of the frequency of ON-center and OFF-center varieties, an asymmetry not present in ganglion cells whose center receives input from the other two cone types. A similar asymmetry of ON/OFF responses is found in the local electrotetinogram (d-wave) mediated by signals from blue-sensitive cones. ‘Blue-ON-center’ ganglion cells have larger receptive-field centers and shorter conduction latencies than other opponent-color varieties, suggesting an appreciable degree of receptor convergence and presumably large cell bodies. Intracellular stainings of these neurons with Procion Yellow show that they correspond to diffuse stratified (Parasol) ganglion cells whose flat-topped dendritic arborization stratifies in the sclerad half of the inner plexiform layer. In view of the known characteristics of macaque bipolar cells and of the ON/OFF asymmetry, it is proposed that these ganglion cells are postsynaptic to cone-specific flat bipolars possibly mediating sign-inverting synaptic contacts. The results also indicate a reversal, for the blue-cone pathway, of the ON/OFF lamination of the inner plexiform layer that has recently been described in other species.

Concealed colour opponency in ganglion cells of the rhesus monkey retina.

Criteria for distinguishing colour‐opponent from spectrally non‐opponent cells and identifying colour‐opponent subtypes on the basis of the cone inputs they receive, have been examined in ganglion cells of the macaque retina using threshold and suprathreshold stimuli, with and without chromatic adaptation. 2. Criteria based on suprathreshold responses were found to be insufficient for distinguishing between opponent and non‐opponent cells in one‐third of the sample. Criteria based on a 560 nm neutral point were found to be insufficient for distinguishing between colour‐opponent subtypes in one‐half of the remaining cells. 3. The neutral point of colour‐opponent ganglion cells varies with the geometry and intensity of the stimulus, as well as with the amount of centre‐surround interaction and the receptive‐field location of a cell. As a result, the neutral point is often an ambiguous criterion for identifying colour‐opponent subtypes on the basis of their cone inputs. 4. About one third of the colour‐opponent ganglion cells did not show colour opponency in the presence of neutral backgrounds, and only revealed this behaviour in the presence of chromatic adaptation (concealed colour opponency). 5. The proportion of these concealed colour‐opponent cells increased towards the peripheral areas of the retina.

Regularity and Structure of the Spatial Pattern of Blue Cones of Macaque Retina

Abstract Models were developed for describing the regular pattern of blue cones in macaque retina. Two functional descriptions were applied to patterns, one based on the cdf of interpoint distances, the other on the cdf of the central angles of Voronoi regions. Disordered triangular and square lattices and hard balls failed to model the blue-cone point pattern. An elastic-ball model was developed whose spatial properties fit well those of the blue-cone pattern. This model employed a hard core and a soft surrounding shell and is proposed as a valid model for the blue-cone pattern.

Spectral interactions in horizontal and ganglion cells of the isolated and arterially-perfused rabbit retina.

Summary Intracellular and extracellular recordings in the arterially-perfused eye cup of pigmented and albino rabbits show the presence of blue cones, green and rods. Among the ganglion cells, a fraction shows spectral opponency. Two main types were found. In one, on-depolarizing responses and on-hyperpolarizing responses receive antagonistic input from different cone type (‘B/G’); in the other, on-depolarizing responses receive input from both blue and green cones whereas off-depolarizing responses receive input either from blue or from green cones (‘BG/G’, ‘BG/B’). Two types of horizontal cell responses have been found, both receiving mixed green cone and rod input; one type is cone-dominated while the other is rod-dominated. Neither type shows C-type responses or obvious input from blue cones, either synergistic or antagonistic, with intense selective chromatic adaptation of green cones and rods. Mass b-wave responses show a spectral sensitivity suggestive of antagonistic interactions between blue and green cones signals to inner nuclear layer neurones, which were not seen in action spectra based on a-wave or PII component responses. It is argued that although blue cone signals contribute to spectral interactions at the ganglion cell and inner nuclear layer cell levels, they do not seem to contribute significantly to such interactions at the receptor or horizontal cell levels.

Protan‐like spectral sensitivity of foveal Y ganglion cells of the retina of macaque monkeys.

1. The spectral sensitivity of two varieties of macaque Y ganglion cells with a centre‐surround organization, type III (non‐colour opponent) and type IV (broad‐band colour opponent), was examined with test stimuli of different size, shape and wave‐length. 2. The spectral sensitivity of type III cells to large stimuli decreased at the long wave‐lengths with decreasing retinal eccentricity; this change was due to a lower sensitivity of green‐sensitive than of red‐sensitive cone input to the surround of foveal cells, which resulted in stronger surround antagonism at the long than at the short wave‐lengths leading to a rudimentary form of colour opponency. 3. The spectral properties of foveal type III cells were intermediate between those of perifoveal type III cells, whose surrounds receive a rather similar input from both cone types, and of the predominantly foveal type IV cells, whose surrounds appeared to lack input from green‐sensitive cones. 4. The results indicate that both cell types represent varieties within a continuum of a single macaque Y‐cell system which has a reduced long‐wave‐length sensitivity in the foveal region. The fact that a similar reduction of long‐wave‐length sensitivity can be observed in (foveal) macaque photopic luminosity functions measured with different techniques by different authors suggest that both types of Y cell have an important role in the processing of luminance information.

Spatial summation, response pattern and conduction velocity of ganglion cells of the rhesus monkey retina

Enroth-Cugell and Robson (1966) described two classes of ganglion cells in the retina of the cat, which were independent of the on-centre/off-centre class& cation (KufHer, 1953). On the basis of responses to drifting parallel gratings with the highest spatial frequency capable of eliciting a response, the neurones were divided into Xand Y-cells: the former always showed a modulation of firing at the drift frequency. while the latter showed an unmodulated increase in the mean discharge. A number of cells of both types were also distinguished by the presence or absence of a null position for a stationary grating of low spatial frequency, at which the introduction or removal of the pattern yielded no significant response. This observation suggested that the spatial summation of X-cells was linear and that of Y-cells was non-linear (cf. Enroth-Cugell and Robson, 1966). Several reports have recently classed ganglion cells mainly on the basis of the time course of responses to maintained stimuli as well as conduction velocity (Cleland, Dubin and Levick, 1971; Fukada, 1971: Ikeda and Wright. 1972; Stone and Hoffman, 1972; Cleland, Levick and Sanderson, 1973; Cleland and Levick, 1974; Stone and Fukuda, 1974). Despite accomplished variations in nomenclature, three main classes of cells appear to have been distinguished in most of these studies. Some cells having transient responses or fast conduction velocity have been equated to Y-cells, while other cells with sustained responses or slow conduction velocity have been equated to X-cells. A third group of cells has been distinguished mostly on the basis that their conduction velocity was much slower (Stone and Fukuda, 1974) or their responses less brisk (CleLand and Levick, 1974) than those of cells equated to Xand Y-cells. The functional significance of these “W-cells” is somewhat obscured by their heterogeneity and by the controversy of whether they represent a tertium quid of the X/Y dichotomy or the basis for another dichotomy independent of the X,IY one. None of these Studies. however. have conclusively proved the postulated correspondence between classifications based on the response pattern and/or conduction velocity and that based on the linearity of the spatial summation over the receptive field. Gouras (1968. 1969) described two classes of ganglion cells in the retina of the rhesus monkey. Cells with colour-opponent properties had sustained responses (tonic) and slow conduction v-elocities, while spectrally non-opponent cells had transient responses (phasic) and fast conduction velocities. More recently. more classes and varieties of cells were described in this retina (de Monasterio and Gouras. 1975); some of these cells had colour-opponent properties but transient responses while other cells had trigger features or responses departing from the typica ones of -simple” ganglion cells. resembling the results obtained in the retina of the cat. The results reported here represent preliminary information on the linearity of the responses of macaque ganglion cells, and was directed toward a closer look of the relation between spatial summation over the receptive field, on the one hand, and reponse pattern or conduction velocity, on the other hand. Recordings were obtained in the central 20” of the retinae of adult rhesus monkeys, lightly anaesthetised with either sodium pentobarbitone (35 mg/kghr. i.v. infusion) or ketamine hydrochloride (j-20 mg/kghr. i.v. infusion), paralysed with gallamine triethiodide (15-30 mg/kyhr, i.v. infusion) and artificially respired. Rectal temperature. mean arterial pressure, ECG and expired CT& were monitored and maintained within normal values. Anaesthetic level and dosage were assessed by cortical EEG monitoring (stage II wave form) of the posterior temporal-occipital derivation; brisk reflexes but no organised responses were

Responses of macaque ganglion cells to far violet lights

Abstract In a sample of 487 colour-opponent ganglion cells recorded in the central retina of the rhesus and cynomolgus monkeys, 9% of these neurones were found to have responses with the same sign at both ends of the visible spectrum mediated by red-sensitive cones and mid-spectral responses of opposite sign mediated by green-sensitive cones. Selective chromatic adaptation showed that the responses to far violet lights (400–420 nm) were due to input from red- and not blue-sensitive cones. These responses were enhanced by backgrounds depressing the sensitivity of blue- and green-sensitive cones and they were depressed by backgrounds depressing the sensitivity of red-sensitive cones; the sensitivity of these responses was yoked to that of responses to far red lights. The relative incidence of these ganglion cells was maximal at the foveal region and decreased towards the peripheral retina. The properties of these cells are consistent with some psychophysical observations of human vision at the short wave-lengths.

Signals from blue cones in “red-green” opponent-colour ganglion cells of the macaque retina

Abstract Many opponent-colour ganglion cells of the macaque retina overt input from green and red-sensitive cones but often appear to lack input from blue-sensitive cones under usual test conditions. Comparisons of field and test action spectra of the responses of a selected group of such “red-green” ganglion cells, located in the perifovea and lacking rod input, indicate the presence of blue-sensitive cone signals having a suppressive influence upon the more direct and opponent signals from green- and red-sensitive cones to a fraction of these neurones, which seems to take place at a level distal to that of the ganglion cell. No cell excitation of inhibition mediated by blue-sensitive cone signals could be observed on intense yellow-adapting lights desensitizing the other two cone types. These neurones are characterized by a sharp fall-off in their short-wavelength test sensitivity and by a secondary shoulder in their short-wavelength field sensitivity. In addition, when cell responses overtly mediated by input from green-sensitive cones are depressed by the geometry of the stimuli, the suppressive signals from blue-sensitive cones also result in a large displacement towards the short wavelengths of the test peak sensitivity of such responses. This displacement can be described with acceptable accuracy by a two-stage model based on subtractive interactions between A1-photopigments with λmax at 445, 535 and 570 nm, which is qualitatively consistent with other spectral properties of these ganglion cells.