Parvocellular Cells Research Articles

Spatial Frequency and the Magno-Parvocellular Distinction—Some Remarks

Many researchers have attempted to use suprathreshold contrast stimuli of low or high spatial frequencies to selectively stimulate (or bias stimuli for) the magnocellular or parvocellular subcortical visual pathways. While this can be done at contrast threshold, the possibility of doing so at suprathreshold contrasts is less clear and is reviewed here. Research on monkeys indicates that (1) magno-and parvocellular neurons are similar when compared at the same visual field eccentricity. Also, (2) koniocellular neurons seem comparable to magno-and parvocellular cells with regard to spatial properties. In addition, (3) cortical neurons are highly selective for spatial frequencies making it possible that response differences associated with high and low spatial frequencies reflect cortical rather than subcortical factors. It is concluded, that the manipulations of spatial frequency in suprathreshold stimuli provides a poor means for separating the magnocellular and parvocellular systems.

The temporal properties of the response of macaque ganglion cells and central mechanisms of flicker detection

This analysis assesses sensitivity of primate ganglion cells to sinusoidal modulation as a function of temporal frequency, based on the structure of their impulse trains; sensitivity to luminance and chromatic modulation was compared to human psychophysical sensitivity to similar stimuli. Each stimulus cycle was Fourier analyzed, and response amplitudes subjected to neurometric analysis; this assumes a detector with duration inversely proportional to frequency, that is, the stimulus epoch analyzed is a single cycle rather than a fixed duration, and provides an upper bound for a detection by an observer who bases judgments on a single cell. Signal-to-noise ratio for a given Fourier amplitude rapidly decreased with temporal frequency. This is a consequence of the statistics of impulse trains making up the response; at higher temporal frequencies, there are fewer impulses per cycle. Performance of this "single-cell" observer was then compared with that of modeled central detection mechanisms of fixed duration. For chromatic modulation, a filter/detector with a time constant of approximately 40 ms operating upon the parvocellular (PC) pathway provided a match to psychophysical results, whereas for luminance modulation, a filter/detection mechanism operating upon the magnocellular (MC) pathway with a time constant of approximately 5-10 ms provided a suitable match. The effects of summation and nonlinear interactions between cell inputs to detection are also considered in terms of enhanced sensitivity and "sharpness" of thresholds, that is, the steepness of the neurometric function. For both luminance (MC cells) and chromatic modulation (PC cells), restricted convergence (<20 cells) appears adequate to provide sharp thresholds and sensitivity comparable to psychophysical performance.

Spatial receptive field properties of lateral geniculate cells in the owl monkey (Aotus azarae) at different contrasts: a comparative study

Several physiological properties of owl monkey lateral geniculate nucleus (LGN) cells were studied to verify whether its nocturnal habit has an influence on the organization of its subcortical visual system. Receptive field (RF) dimensions were measured using drifting gratings and bipartite field stimuli. We found that owl monkey cells LGN have larger RFs and were on average more non-linear than those of diurnal monkeys. But, as in other anthropoids, there is an increase in RF centre size with increasing eccentricity, and there is a limited correlation between these centre sizes and retinal ganglion cell dendritic tree sizes. The influence of contrast on sizes and peak sensitivities of RF centres and surrounds and on the response phases was studied. Both the sizes and peak sensitivities of the RF centres and surrounds decrease as contrast increases. As a result, the responses to low spatial frequency stimuli saturate with increasing contrast. Estimates of contrasts at half-maximal responses confirm the presence of saturation. It was found that the magnocellular cells saturate more strongly than parvocellular cells. The response phase increases with increasing contrast. These data resemble those obtained in the common marmoset, indicating that these are basic features of the primate visual system. We conclude that during evolution and as an adaptation to a nocturnal lifestyle, cells in the owl monkey LGN display an increased spatial integration in comparison with diurnal primate species, without a change in the basic organization common to the primate subcortical visual system.

Plastic changes induced by neonatal handling in the hypothalamus of female rats

Early-life events can exert profound long-lasting effects on several behaviors such as fear/anxiety, sexual activity, stress responses and reproductive functions. Present study aimed to examine the effects of neonatal handling on the volume and number of cells in the hypothalamic paraventricular nucleus (pPVN, parvocellular and mPVN, magnocellular regions) and the supraoptic nucleus (SON) in female rats at 11 and 90 days of age. Moreover, in the same areas, immunohistochemistry for oxytocin (OT) and glial fibrillary acidic protein (GFAP) were analyzed in the adult animals. Daily handling during the first 10 postnatal days reduced the number of cells in the pPVN and SON at both the 11 and 90 days. Handling decreased the number of OT-positive parvocellular cells in the PVN in adult females. No significant differences were detected on the optical density (OD) of GFAP-positive cells between the handled and nonhandled adult females. The effect of handling on cell loss was observed 24 h after the 10-day handling period and persisted into adulthood, indicating a stable morphological trace. Results suggest that neonatal handling can induce plastic changes in the central nervous system.

Response variability of marmoset parvocellular neurons

This study concerns the properties of neurons carrying signals for colour vision in primates. We investigated the variability of responses of individual parvocellular lateral geniculate neurons of dichromatic and trichromatic marmosets to drifting sinusoidal luminance and chromatic gratings. Response variability was quantified by the cycle-to-cycle variation in Fourier components of the response. Averaged across the population, the variability at low contrasts was greater than predicted by a Poisson process, and at high contrasts the responses were approximately 40% more variable than responses at low contrasts. The contrast-dependent increase in variability was nevertheless below that expected from the increase in firing rate. Variability falls below the Poisson prediction at high contrast, and intrinsic variability of the spike train decreases as contrast increases. Thus, while deeply modulated responses in parvocellular cells have a larger absolute variability than weakly modulated ones, they have a more favourable signal: noise ratio than predicted by a Poisson process. Similar results were obtained from a small sample of magnocellular and koniocellular ('blue-on') neurons. For parvocellular neurons with pronounced colour opponency, chromatic responses were, on average, less variable (10-15%, p<0.01) than luminance responses of equal magnitude. Conversely, non-opponent parvocellular neurons showed the opposite tendency. This is consistent with a supra-additive noise source prior to combination of cone signals. In summary, though variability of parvocellular neurons is largely independent of the way in which they combine cone signals, the noise characteristics of retinal circuitry may augment specialization of parvocellular neurons to signal luminance or chromatic contrast.

Do magnocellular and parvocellular ganglion cells avoid short-wavelength cone input?

We recently developed a new technique to measure cone inputs to visual neurons and used this technique to seek short-wavelength-sensitive (S) cone inputs to parasol, magnocellular (MC) and midget, parvocellular (PC) ganglion cells. Here, we compare our physiological measurements of S-cone weights to those predicted by a random wiring model that assumes cells' receptive fields receive input from mixed cone types. The random wiring model predicts the average weights of S-cone input to be similar to the total percentage of S-cones but with considerable scatter, and the S-cone input polarity to be consistent with that of PC cells' surround and of MC cells' center. This is not consistent with our physiological measurements. We suggest that the ganglion cells' receptive fields may have a mechanism to avoid S-cone inputs, as is the case in the H1 horizontal cells. Previous reports of S-cone inputs, in particular substantial input to MC cells, are likely to reflect variation in prereceptoral filtering and/or the failure to correct for variation in macular pigment.

Contribution of chromatic aberrations to color signals in the primate visual system

We measured responses to red-green color variation in parvocellular (PC) neurons in the lateral geniculate nucleus of dichromatic ("red-green color blind") marmoset monkeys. Although these animals lack distinct visual pigments to distinguish between wavelengths in this range, many of the colored stimuli nevertheless produced robust responses in PC cells. We show that these responses, which are restricted to high stimulus spatial frequencies (fine image details), arise from chromatic aberrations in the eye. The neural signals produced by chromatic aberrations are of comparable magnitude to signals produced by high-frequency luminance (LUM) modulation and thus could influence cortical pathways for processing of color and object recognition. The fact that genetically "color-blind" primates are not necessarily blind to wavelength-dependent contours in the visual world may have enabled red-green color vision to become linked with high-acuity spatial vision during primate evolution.

Xylazine activates oxytocinergic but not vasopressinergic hypothalamic neurons under normal and hyperosmotic conditions in rats

Role of central alpha2-adrenoceptors in the regulation of hypothalamic magnocellular cells was studied under hyperosmotic challenge elicited by hypertonic saline (HS). Rats pretreated with receptor agonist, xylazine (XYL), were injected intraperitoneally with different (low: 0.375, moderate: 0.75, high: 1.5 M) HS 30 min later. The activity of the paraventricular (PVN) and supraoptic (SON) vasopressin and oxytocin perikarya was established by Fos–dual-immunohistochemistry 60 min after HS administration. Results showed that 1/XYL is a potent stimulus for oxytocin but not vasopressin magnocellular cells under basal and weak hyperosmotic conditions 2/highHS completely overlaps the effect of XYL. In addition, XYL partially suppressed Fos expression in the parvocellular PVN cells activated by highHS. The data suggest that alpha2-adrenoceptors may play an important role in the regulation of oxytocinergic PVN and SON neurons under basal and weak hyperosmotic conditions and that alpha2-adrenoceptors may also participate in the control of PVN parvocellular cells under intense osmotic challenge.

Differential actions of acute and chronic citalopram on the rodent hypothalamic–pituitary–adrenal axis response to acute restraint stress

Serotonin re-uptake inhibitors (SSRIs) can affect the basal activity of the hypothalamic-pituitary-adrenal (HPA) axis in rats. A single injection of citalopram has been shown to stimulate the HPA axis while repeated administration leads to attenuation of the corticosterone response to the SSRI. The purpose of this work was to investigate the rodent HPA axis response to restraint stress, following acute and chronic treatment with the SSRI citalopram. We have demonstrated that a single injection of citalopram is able to prolong acute restraint-induced increases in plasma levels of corticosterone and adrenocorticotrophin (ACTH). This is possibly mediated by arginine vasopressin (AVP) in the parvocellular cells of the paraventricular nucleus (pPVN), as treatment with citalopram or restraint alone did not increase AVP mRNA in pPVN while the combination of treatments resulted in a significant increase in AVP mRNA in the pPVN. In contrast, the increase in corticotrophin-releasing factor (CRF) mRNA in the pPVN in response to acute restraint stress was not altered by citalopram. Oxytocin (OT) mRNA was also increased in the magnocellular PVN (mPVN) by the solo treatments of citalopram and restraint, and was not further enhanced by the dual treatment of restraint and citalopram. Chronic treatment with citalopram did not alter basal plasma levels of corticosterone or ACTH. However, the ACTH response to acute restraint was attenuated following chronic citalopram treatment. AVP mRNA in the pPVN was significantly elevated in response to chronic citalopram compared with saline controls suggesting an effect mediated through the AVP subset of pPVN neurones. The CRF mRNA response to acute restraint was not altered in rats treated chronically with citalopram. OT mRNA was not enhanced in the mPVN following chronic infusion of citalopram but was increased by acute restraint stress. We conclude from these data that both acute and chronic citalopram treatment has the potential to alter the rodent response to acute restraint stress. These effects appear to be regulated by the AVP-containing subset of CRF neurons in the pPVN and thus suggest that parvocellular AVP may have an important role in mediating the actions of SSRIs.

Chromatic Gain Controls in Visual Cortical Neurons

Although the response of a neuron in the visual cortex generally grows nonlinearly with contrast, the spatial tuning of the cell remains stable. This is thought to reflect the activity of a contrast gain control ("normalization") that has very broad tuning on the relevant stimulus dimension. Contrast invariant tuning on a particular dimension is probably necessary for reliable representation of stimuli on that dimension. In the lateral geniculate nucleus (LGN), V1, and V2 of anesthetized macaque, we measured chromatic tuning of neurons at several contrasts to characterize the gain controls and identify cells that might be important for representing color. We estimated separately the chromatic signature of the linear receptive field and that of the gain control. In the LGN, we found normalization in magnocellular cells and cells receiving excitatory S-cone input but not in parvocellular cells or those receiving inhibitory S-cone input. We found normalization in all types of cortical neurons. Among cells that preferred achromatic modulation, or modulation along intermediate directions in color space (making them responsive to both achromatic and chromatic stimuli), normalization was driven by mechanisms tuned to a restricted range of directions in color space, close to achromatic. As a result, chromatic tuning varied with contrast. Among the relatively few cells that strongly preferred chromatic modulation, normalization was driven by mechanisms sensitive to modulation along all directions in color space, especially isoluminant. As a result, chromatic tuning changed little with contrast. To the extent that contrast invariant tuning is important in representing chromaticity, relatively few cortical neurons are involved.

Chromatic Organization of Ganglion Cell Receptive Fields in the Peripheral Retina

This study addresses the chromatic properties of receptive fields in the subcortical visual pathway of primates. There is agreement that, in the central visual field, many cells belonging to the parvocellular (PC) division of the subcortical pathway show red-green opponent responses, that a subgroup of cells belonging to the koniocellular (KC) pathway shows blue-yellow opponent responses, and that magnocellular (MC) pathway cells show only weak signs of chromatic input. However, the chromatic properties of ganglion cells in the peripheral retina are poorly understood. Here, we measured the temporal-chromatic properties of ganglion cells in extracellular in vivo recordings from peripheral macaque retina. We show that the chromatic responsivity of peripheral KC ("blue-on") and MC cells is very similar to that of their counterparts in the foveal retina. Cone-opponent responses are expressed only at low temporal frequencies (<10 Hz) in the majority of peripheral PC cells, and some peripheral PC cells show non-opponent response properties. With these exceptions, the chromatic properties of ganglion cells are essentially preserved throughout the first 50 degrees of visual eccentricity. The main change seen in passing from foveal to peripheral retina is that all ganglion cell classes become more responsive to high temporal-frequency modulation.

Neuroprotective effect of rasagiline, a monoamine oxidase-B inhibitor, on spontaneous cell degeneration in a rat model

Spontaneously hypertensive rats (SHR) pathologically elevate blood pressure with age. This elevation is accompanied by specific neuronal degeneration in the hypothalamus and enlargement of the lateral ventricles. The aim of this study was to assess the neuroprotective effect of the monoamine oxidase B (MAO-B) inhibitor, rasagiline on paraventricular (PVN) hypothalamic degeneration in SHR. The S-enantiomer of rasagiline, S-PAI, a much weaker MAO inhibitor, and two antihypertensive drugs, captopril and hydralazine were also tested. Normotensive Wistar Kyoto (WKY) rats served as controls. One month-old SHR or WKY rats were treated daily for 3-4 months. Systolic blood pressure was recorded, parvocellular vasopressin (VP) immunopositive cells were counted and the area of the third ventricle measured. In saline-treated SHR, blood pressure rose significantly and the number of VP parvocellular cells was reduced by about 60% relative to WKY. Rasagiline, 1 mg/kg/day, reduced PVN neuronal cell death in SHR up to 112% relative to saline-treated SHR; 0.3 mg/kg/day exerted a smaller but significant effect. These actions were accompanied by parallel reductions in systolic blood pressure. Captoril, hydralazine and S-PAI did not prevent death of VP neurons. In SHR, the volume of the third ventricle was about double that of WKY. Rasagiline significantly prevented this ventricular dilation. These results indicate than rasagiline protects from cell death in an in vivo animal model in a dose-dependant manner and could be of use as a neuroprotector in the central nervous system.

Profound Contrast Adaptation Early in the Visual Pathway

Summary has investigated slow contrast adaptation in the primate retina, and that found substantially less adaptation than Prior exposure to a moving grating of high contrast led to a substantial and persistent reduction in the in the salamander. We describe here new observations that sharply clarify the picture in the primate visual pathcontrast sensitivity of neurons in the lateral geniculate nucleus (LGN) of macaque. This slow contrast adapta- way and have major implications for psychophysical studies: neurons in magnocellular LGN (M cells), but tion was potent in all magnocellular (M) cells but essentially absent in parvocellular (P) cells and neurons not those in parvocellular LGN (P cells), show strong contrast adaptation that originates in the retina. that received input from S cones. Simultaneous recordings of M cells and the potentials of ganglion cells driving them showed that adaptation originated in gan- Results glion cells. As expected from the spatiotemporal tuning of M cells, adaptation was broadly tuned for spatial Aftereffects of Adaptation to High-Contrast Stimuli frequency and lacked orientation selectivity. Adapta- We studied the responses of single neurons in LGN tion could be induced by high temporal frequencies of anesthetized macaque before, during, and through to which cortical neurons do not respond, but not by recovery from adaptation to contrast modulation of diflow temporal frequencies that can strongly adapt cor- ferent stimuli. Our initial experiments were prompted tical neurons. Our observations confirm that contrast by observations in ganglion cells (Baccus and Meister,

Chromatic and spatial properties of parvocellular cells in the lateral geniculate nucleus of the marmoset (Callithrix jacchus).

The parvocellular (PC) division of the afferent visual pathway is considered to carry neuronal signals which underlie the red-green dimension of colour vision as well as high-resolution spatial vision. In order to understand the origin of these signals, and the way in which they are combined, the responses of PC cells in dichromatic ('red-green colour-blind') and trichromatic marmosets were compared. Visual stimuli included coloured and achromatic gratings, and spatially uniform red and green lights presented at varying temporal phases and frequencies.The sensitivity of PC cells to red-green chromatic modulation was found to depend primarily on the spectral separation between the medium- and long-wavelength-sensitive cone pigments (20 or 7 nm) in the two trichromatic marmoset phenotypes studied. The temporal frequency dependence of chromatic sensitivity was consistent with centre-surround interactions. Some evidence for chromatic selectivity was seen in peripheral PC cells. The receptive field dimensions of parvocellular cells were similar in dichromatic and trichromatic animals, but the achromatic contrast sensitivity of cells was slightly higher (by about 30%) in dichromats than in trichromats. These data support the hypothesis that the primary role of the PC is to transmit high-acuity spatial signals, with red-green opponent signals appearing as an additional response dimension in trichromatic animals.

Profound Contrast Adaptation Early in the Visual Pathway

Prior exposure to a moving grating of high contrast led to a substantial and persistent reduction in the contrast sensitivity of neurons in the lateral geniculate nucleus (LGN) of macaque. This slow contrast adaptation was potent in all magnocellular (M) cells but essentially absent in parvocellular (P) cells and neurons that received input from S cones. Simultaneous recordings of M cells and the potentials of ganglion cells driving them showed that adaptation originated in ganglion cells. As expected from the spatiotemporal tuning of M cells, adaptation was broadly tuned for spatial frequency and lacked orientation selectivity. Adaptation could be induced by high temporal frequencies to which cortical neurons do not respond, but not by low temporal frequencies that can strongly adapt cortical neurons. Our observations confirm that contrast adaptation occurs at multiple levels in the visual system, and they provide a new way to reveal the function and perceptual significance of the M pathway.

The spatiotemporal precision of ganglion cell signals: a comparison of physiological and psychophysical performance with moving gratings

Comparison of the spatiotemporal information delivered by ganglion cells with human psychophysical performance may give insight to how retinal information is utilized by cortical mechanisms, and constrain models of spatiotemporal processing. Ganglion cells’ responses were measured with drifting gratings of various spatial and temporal frequencies and contrasts. The spatiotemporal precision of cell responses was estimated in terms of a noise measure and phase variation, and compared to human vernier performance. Noise and phase variation of magnocellular (MC) cells was least at low temporal frequencies, despite their transient responses. The patterns of spatiotemporal precision of MC cells resembled the patterns of human vernier thresholds while those of parvocellular cells did not, implying use of MC cells’ signals in these tasks. The analysis further implied that cortical mechanisms must perform a sophisticated spatiotemporal analysis over local ganglion cell arrays.

Human temporal impulse response speeds up with increased stimulus contrast

It is well known that raising mean luminance speeds-up the visual response to temporal change. At higher mean luminance, the temporal impulse response function (IRF) becomes more transient or biphasic. An analogous effect is observed physiologically when stimulus contrast is increased, at constant mean luminance. As stimulus contrast is raised, the temporal response to flicker advances in phase and becomes more transient (bandpass). The MC (magnocellular) retinal ganglion cells manifest this temporal contrast gain control, but the PC (parvocellular) cells do not. We show psychophysically that the temporal response in humans speeds-up in an analogous manner as stimulus contrast is raised. Low spatial-frequency gratings, of suprathreshold contrast, were presented as pairs of pulses, separated by brief delays. Responses became more transient with increasing contrast in both our motion task (direction discrimination) and in our flicker task (‘agitation’ discrimination), mimicking the temporal contrast gain control seen in the physiological studies. Results could be modeled with a nonlinearity, in which the IRF shortens with increasing contrast.

Processing of Natural Temporal Stimuli by Macaque Retinal Ganglion Cells

This study quantifies the performance of primate retinal ganglion cells in response to natural stimuli. Stimuli were confined to the temporal and chromatic domains and were derived from two contrasting environments, one typically northern European and the other a flower show. The performance of the cells was evaluated by investigating variability of cell responses to repeated stimulus presentations and by comparing measured to model responses. Both analyses yielded a quantity called the coherence rate (in bits per second), which is related to the information rate. Magnocellular (MC) cells yielded coherence rates of up to 100 bits/sec, rates of parvocellular (PC) cells were much lower, and short wavelength (S)-cone-driven ganglion cells yielded intermediate rates. The modeling approach showed that for MC cells, coherence rates were generated almost exclusively by the luminance content of the stimulus. Coherence rates of PC cells were also dominated by achromatic content. This is a consequence of the stimulus structure; luminance varied much more in the natural environment than chromaticity. Only approximately one-sixth of the coherence rate of the PC cells derived from chromatic content, and it was dominated by frequencies below 10 Hz. S-cone-driven ganglion cells also yielded coherence rates dominated by low frequencies. Below 2-3 Hz, PC cell signals contained more power than those of MC cells. Response variation between individual ganglion cells of a particular class was analyzed by constructing generic cells, the properties of which may be relevant for performance higher in the visual system. The approach used here helps define retinal modules useful for studies of higher visual processing of natural stimuli.

Modulation sensitivity of ganglion cells in peripheral retina of macaque

There is ample psychophysical evidence that flicker is more salient in the peripheral than the central visual field, but the physiological basis of this eccentricity-dependant change is unclear. Here, we compared responsivity to temporal modulation of ganglion cells in central and peripheral primate retina. Above 30 Hz modulation frequency, both magnocellular (MC) and parvocellular (PC) pathway cells are more responsive in peripheral retina. This suggests that an increase in high-frequency temporal responsiveness arises in outer retina before the MC and PC pathways diverge. In both central and peripheral retina, the critical fusion frequency of MC cells is higher than that of PC cells. This result is consistent with other evidence that psychophysical flicker sensitivity is mediated by the MC pathway.

Extraclassical Receptive Field Properties of Parvocellular, Magnocellular, and Koniocellular Cells in the Primate Lateral Geniculate Nucleus

Descriptions of receptive fields at subcortical levels of the visual system have mostly considered only the classical receptive field (CRF). A suppressive extraclassical receptive field (ECRF) has been demonstrated in relay cells within the primate lateral geniculate nucleus (LGN), but the quantitative properties and specific influence of the ECRF on the distinct magnocellular (MC), koniocellular (KC), and parvocellular (PC) pathways are not known. Here we quantified the effect of ECRF stimulation on visually responsive cells in the LGN of a diurnal New World primate, the marmoset. We show that for all cells, visually evoked responses are reduced by stimulation of the ECRF. The magnitude of the suppression is greatest for MC cells and smallest for PC cells. The effect of ECRF stimulation on KC cells is variable but always suppressive. We refer to these effects as extraclassical inhibition (ECI). The contrast-response relationship of the ECI parallels that of CRF-induced excitation for each cell class: for MC cells, ECI contrast threshold is close to 10% and the ECI saturates at 50% contrast, but the contrast dependence of ECI on PC cells is more linear. The ECI also contributes to contrast-dependent changes in spatial summation: on average for all LGN cells the radius of the excitatory spatial summation field (measured from aperture-tuning curves) at low contrast is 1.31 times that at high contrast. No consistent effects of orientation on ECI were seen. The data suggest that the suppressive component of the ECRF seen in cortical neurons could primarily be inherited from subcortical input streams.