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The Journal of Neurophysiology Vol. 80 No. 4 October 1998, pp. 2063-2076
Copyright ©1998 by the American Physiological Society
Department of Physiology and Institute for Biomedical Research, The University of Sydney, New South Wales 2006, Australia
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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White, Andrew J. R., Heath D. Wilder, Ann K. Goodchild, Ann Jervie Sefton, and Paul R. Martin. Segregation of receptive field properties in the lateral geniculate nucleus of a New-World monkey, the marmoset Callithrix jacchus. J. Neurophysiol. 80: 2063-2076, 1998. The lateral geniculate nucleus (LGN) in humans and Old-World monkeys is dominated by the representation of the fovea in the parvocellular (PC) layers, and most PC cells in the foveal representation have red-green cone opponent receptive field properties. It is not known whether these features are both unique to trichromatic primates. Here we measured receptive field properties and the visuotopic organization of cells in the LGN of a New-World monkey, the marmoset Callithrix jacchus. The marmoset displays a polymorphism of cone opsins in the medium-long wavelength (ML) range, which allows the LGN of dichromatic ("red-green color blind") and trichromatic individuals to be compared. Furthermore, the koniocellular-interlaminar layers are segregated from the main PC layers in marmoset, allowing the functional role of this subdivision of the LGN to be assessed. We show that the representation of the visual field in the LGN is quantitatively similar in dichromatic and trichromatic marmosets and is similar to that reported for macaque; the vast majority of LGN volume is devoted to the central visual field. ON- and OFF-type responses are partially segregated in the PC layers so that ON responses are more commonly encountered near the external border of each layer. The red-green (ML) opponent cells in trichromatic animals were all located in the PC layers, and their receptive fields were within 16° of the fovea. The koniocellular zone between the PC and magnocellular layers contained cells that receive excitatory input from short wavelength sensitive cones ("blue-ON cells") as well as other nonopponent cells. These results suggest that the basic organization of the LGN is common to dichromatic and trichromatic primates and provide further evidence that ML and SWS opponent signals are carried in distinct subdivisions of the retinogeniculocortical pathway.
The lateral geniculate nucleus (LGN) of anthropoid primates is normally described as consisting of two major subdivisions, the parvocellular (PC) layers and the magnocellular (MC) layers, separated by sparsely populated interlaminar or koniocellular zones. The bulk of the LGN in these species is devoted to the representation of the foveal retina in the PC layers (Connolly and Van Essen 1984
Physiological measurements
Recordings were made from 10 adult marmosets (Callithrix jacchus), body weight 250-370 g. Animals were obtained from the Australian Commonwealth Scientific and Industrial Research Organization/National Health and Medical Research Council of Australia combined breeding facility in Adelaide. Three of the animals were male; the others were female. In this study we describe in detail the results obtained from seven female animals from which complete anatomic reconstructions of the LGN were made. All procedures used are approved by the University of Sydney Institutional Animal Care and Ethics committee and conform with the provisions of the Australian NHMRC code of practice for the care and use of animals. The animals were anesthetised with a mixture of xylazine (~0.3 mg/kg im) and ketamine (30 mg/kg im) for surgery. Anesthesia was maintained with isoflurane (2% during surgical procedures, 0.25-0.75% during recording) and a 70%-30% mixture of NO2:carbogen (5% CO2 in O2). A venous infusion of 40 µg·kg Visual stimuli
Each visually responsive cell was initially classified by using hand-held stimuli; thereafter all stimuli were delivered through a Maxwellian view system (Smith et al. 1992 Tissue preparation
The location of each recorded cell was noted by reading the depth from the hydraulic microelectrode advance (David Kopf Model 640). Electrolytic lesions (6-20 µA × 10-20 s, electrode negative) were made at the location of some cells. At least two lesions were made on each electrode track. If a steel recording electrode was used, some locations were marked by passing positive current for later reaction by the Prussian blue method. At the end of the recording session the animal was killed with an overdose of pentobarbitone sodium (80-150 mg/kg iv) and perfused with intracardially with saline (0.9% NaCl, 0.4 l) followed by freshly prepared 4% paraformaldehyde in 0.1 M phosphate buffer (PB; pH 7.4., 0.5 l) with 10% potassium ferrocyanide. The brain was removed and placed in 30% sucrose in PB until it sank. Serial coronal sections at 30-µm thickness were cut on a freezing microtome, mounted, air dried, stained with cresyl violet, dehydrated, and coverslipped with Ultramount.
Analysis
The analysis was made at two levels of precision. The visuotopic map was established from both single and multiple unit recording sites throughout the LGN. A subset of these recording positions also satisfied the following criteria. The action potential was identified as arising from a single cell body (Bishop et al. 1962 Morphology of the marmoset LGN
Figure 1 shows representative coronal sections through the marmoset LGN. The basic lamination pattern of two PC and two MC layers separated by an interlaminar zone with small cell bodies (Kaas et al. 1978 Visual field representation
We first confirmed the observation of Yeh et al. (1995b)
Foveal magnification
We measured the volume of the LGN that is devoted to each of the visual field zones shown in Fig. 5. For each lamina, the area within each zone was measured. The volume for each zone was calculated with Cavalieri's method (Gundersen and Jensen 1987
Segregation of ON and OFF responses
The first cell encountered in any given electrode penetration usually had an ON-center receptive field. For 27 penetrations, 80% of the first cells encountered in the external PC layer were ON-center cells. We measured the laminar position of cells classified as ON- or OFF- center, both from the response to hand-held stimuli and from the phase of the cells' responses to luminance modulation. Cells showing evidence of input from SWS cones were excluded from this analysis. The results are shown in Fig. 6. There is a slight preponderance of ON-center cells over OFF-center cells in both the PC and magnocellular layers, as reported for macaque (Derrington and Lennie 1984
Distribution of ML cone opponent cells
We examined the distribution of cone opponent response properties within the marmoset LGN. Figure 7 shows examples of cells receiving input from cone mechanisms in the ML range. The responses of two PC cells and one magnocellular cell are compared. Two stimulus paradigms are shown, luminance modulation (Fig. 7A) and equal luminant red-green chromatic modulation (Fig. 7B). The amplitude of the 3.906-Hz Fourier component of each cell's response is shown in Fig. 7C. The majority of PC cells and all magnocellular cells were more responsive to luminance than to chromatic modulation. The results are similar to those described by Yeh et al. (1995b)
Responses and distribution of blue-ON cells
Yeh et al. (1995b)
Visual field representation and retinal topography
Our results show that over one-third of the volume of the marmoset LGN is devoted to the representation of the central 5° of the visual field. As Table 1 shows, this central magnification is at least as great as that reported for macaque (Connolly and van Essen 1984 Segregation of response properties in the PC layers
In macaque, ON-center responses are at least partially localized to the two external PC layers (Derrington and Lennie 1984 Interlaminar zone
The interlaminar zone in marmoset is probably functionally equivalent to the intercalated layers in macaque and other simian primates and to the koniocellular layers in the nocturnal prosimian Galago (for reviews see Casagrande 1994
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
; Le Gros Clark 1941; Malpeli and Baker 1975; Walls 1953). The PC layers have also been associated with the cone opponent responses underlying trichromatic color vision (Derrington et al. 1984; Dreher et al. 1976; Schiller and Colby 1983; Schiller and Malpeli 1978; Wiesel and Hubel 1966). It has been argued that these two features of the primate visual system are interlinked so that the retinal specialization for high spatial resolution foveal vision was a necessary precursor to the evolution of trichromatic color vision (Lennie et al. 1991; Wässle and Boycott 1991).
), tree shrew (Conway and Schiller 1983; Holdefer and Norton 1995), and ferret (Stryker and Zahs 1983)], but evidence for such segregation in the LGN of Old-World primates was so far negative [Galago (Norton and Casagrande 1982)] or equivocal [macaque (Derrington and Lennie 1984; Kaplan and Shapley 1986; Schiller and Malpeli 1978; Wiesel and Hubel 1966)].
, 1996; Jacobs et al. 1996; Mollon et al. 1984; Tovée et al. 1992; Travis et al. 1988; Williams et al. 1992) so that both dichromatic and trichromatic individuals are present (Hunt et al. 1993; Jacobs 1983; Yeh et al. 1995b). The males express a short-wavelength sensitive (SWS) cone pigment and one of three alleles of medium-long wavelength (ML) sensitive pigments, which occupy the same locus on the X chromosome. Heterozygous females, which can express two of these three ML-sensitive pigments, demonstrate behavioral signs of trichromacy (Tovée et al. 1992; Williams et al. 1992). The retina and subcortical visual pathways in marmosets are similar to those described for Old-World primates in both their anatomic (Ghosh et al. 1996; Troilo et al. 1993; Wilder et al. 1996; Yamada et al. 1996) and receptive field properties (Kremers et al. 1997; Martin et al. 1997; Yeh et al. 1995b). The spatial density and connectivity of photoreceptors and ganglion cells in the fovea of the marmoset are quantitatively similar to those in macaque and human (Curcio et al. 1990; Wässle et al. 1989; Wilder et al. 1996), meaning that the species can serve as a useful model for diurnal primate vision.
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FIG. 1.
Coronal sections through the lateral geniculate nucleus (LGN) of a female marmoset at 4 different locations from anterior (A) to posterior (D). Cresyl violet stain. Distance (mm) from the interaural axis is shown at the bottom left of each photomicrograph. Magnocellular layers are not present in the most anterior section (A). All layers can be distinguished most readily in sections through the posterior one-half of the LGN (C and D). Nomenclature according to Kaas et al. (1978) . PE, external parvocellular (PC) layer; PI, internal PC layer; Ipm, interlaminar zone; MI, internal magnocellular (MC) layer; ME, external MC layer. The vertical and horizontal bars in each photomicrograph are 1 mm long. They show distance (in mm) from the midline and depth (in mm) below the surface of the cortex. Section thickness 30 µm.
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FIG. 2.
Retinotopic progression in marmoset LGN. A: camera lucida drawing of the LGN with the reconstructed path of a recording electrode. Location of each cell encountered on the path is indicated. B: receptive field location of cells encountered in this path. Each point shows the center of the receptive field. Open symbols, cells driven by ipsilateral eye; closed symbols, cells driven by contralateral eye. C: same map on an enlarged scale to show the progression of receptive fields near the foveal representation. Receptive fields of cells located at progressively more ventral locations in the lateral aspect of the LGN show a systematic displacement to greater elevations in the visual field.
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FIG. 3.
Composite drawings of the LGN at different coronal levels, showing the location of recorded cells (small squares). Each square is assigned a gray level according to the angle of its receptive field location with respect to the fovea, as indicated by the key diagram at top right. Upper field locations (lighter gray) are located in the lateral aspect of the LGN, and lower field locations (darker gray) are located in the medial aspect of the LGN.
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FIG. 4.
This figure has the same format as Fig. 3. The gray scale shows receptive field eccentricity with respect to the fovea. Fovea is represented in the posterodorsal aspect of each layer of the LGN.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
1·h1 alcuronium chloride (Alloferin, Roche) in dextrose Ringer solution was infused at a rate of 1 ml/h to maintain muscular relaxation. Electroencephalogram and electrocardiogram signals were monitored to ensure adequate depth of anesthesia; in some experiments arterial blood pressure was also monitored by way of a femoral catheter. End-tidal CO2 was measured and maintained near 4% by adjusting the rate and stroke volume of the inspired gas mixture. The pupils were dilated with topical neosynephrine (10%). Penicillin and corticosteroids were administered daily.
, F. Haer, Brunswick, ME) was lowered into the LGN. Action potentials arising from single cells were identified, and the time of their occurrence was measured with an accuracy of 0.1 ms and stored. The visual receptive field location of the multiunit "swish" was also measured at regular intervals throughout the electrode penetration; these measurements were used together with single cell receptive fields to derive the visuotopic map of the LGN.
; Yeh et al. 1995b), which was aligned along the axis of each cell's receptive field and centered on the pupil of the eye. The stimulus in the plane of the pupil was a spatially uniform field composed of the combined image of red, green, and blue light-emitting diodes (LEDs). Temporal waveforms were generated through 12-bit DA converters (NB-A06, National Instruments) under computer control. The LED driver circuitry (Swanson et al. 1987) ensured a linear relationship between driving voltage and LED intensity. The stimulus was calibrated with a PR-650 spectrophotometer (Photo Research, CA). The LED dominant wavelengths were 639, 554, and 470 nm; bandwidth <20 nm at one-half height. An 8-mm aperture was normally placed at the rear focal plane of the Maxwellian view lens to give a stimulus subtense of 6.4°. An artificial pupil was not used. The areal image of the 8-mm aperture was smaller than the diameter of the dilated pupil and thus formed the exit aperture of the optical system. Time-averaged illuminance (measured according to Westheimer 1966) for the red and green LEDs combined was ~1,000 Photopic Trolands; the smaller size of the marmoset eye (Troilo et al. 1993) means that retinal flux per Troland is almost four times higher than for human. Stimuli were normally unattenuated as we wished to minimize the possibility of rod intrusion, which was seen at relatively high levels of retinal illuminance by Yeh et al. (1995b) and Kremers et al. (1996). For some OFF-center cells, responsivity was significantly improved when the stimulus was attenuated by 1 ND.
). The maximum luminance available from the blue LED was 7% that of the red or green, so for this paradigm the red and green amplitude were reduced accordingly. Modulation was between CIE x, y = 0.3, 0.13 and x, y = 0.46, 0.521. The modulation depth of the LED was usually set at 100%. Where the responses showed significant saturation, measurements were also made at 50 or 25% modulation depth.
), the responses of the cell to all three stimulus paradigms described above were measured, and the histological construction allowed the position of the cell to be determined with respect to the laminar borders within the LGN. These cells formed the database for the descriptions of single cell properties.
) with NIH image software. We use the nomenclature of Kaas et al. (1978) for the LGN laminae.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
; Spatz 1978) is most easily seen in the posterior aspect of the LGN (Fig. 1C). In more anterior sections (Fig. 1A) the MC layers are not present. The stereotaxic coordinates indicated for this brain on Fig. 1 are in good agreement with the LGN coordinates from the atlas of the marmoset brain (Stephan et al. 1980). Although there was some variability among animals, we found that electrode penetrations at coordinates anteroposterior 4.0, lateral 6.5 usually passed through the central visual field representation in the LGN. No clear difference in the size or lamination pattern of the LGN was seen between male and female marmosets or between females identified as dichromatic or trichromatic in the recording experiment.
that the visual field map of macaque LGN (Malpeli and Baker 1975) gives a reasonable guide to retinotopic organization in the marmoset LGN. Cells with foveal receptive fields were encountered in penetrations in the posterodorsal aspect of the LGN, with progressively peripheral locations represented in anterior and ventral locations. The progression of receptive field location and eye allegiance for a typical penetration is shown in Fig. 2. As for the macaque (Malpeli and Baker 1975; Malpeli et al. 1996), a line running from the hilum to the genu of the LGN marks the representation of the horizontal meridian. The dorsal visual field is represented on the lateral aspect of the LGN (Fig. 2C, cells 8-13), and the ventral field is represented on the medial aspect of the LGN. The contralateral eye almost always provided the dominant excitatory drive for cells located in the external PC and the internal MC layers. Cells in the internal PC and external MC layers and the majority of cells in the koniocellular zone between the MC and PC layers were driven by the ipsilateral eye. In penetrations through the posterior LGN (foveal representation), we occasionally encountered one or two cells within a lamina that were driven by the "wrong" eye. Their location may correspond to the laminar leaflets revealed by autoradiographic tracing studies in this species (Kaas et al. 1978; Spatz 1978). The electrode path in the ventral part of the LGN was sometimes slightly curved. As reported for macaque by Malpeli et al. (1996), this may be a result of unequal shrinkage.
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FIG. 5.
Summary drawing of the visuotopic map in the marmoset LGN, based on the data shown in Figs. 3 and 4. Visual field zones and their representation in the LGN are shown in different hatch patterns. Anteroposterior distance from the interaural axis (in mm) is indicated above each representative coronal section. Only the PC layers are present at AP level 5.3 mm. Scale bars (1 mm) also show distance from the midline and depth below the cortex (mm) for 1 section.
). Table 1 shows that the PC layers make up~75% of the total laminar volume of the LGN. The total laminar volume of the marmoset LGN (13.09 mm3) is about one-fifth the volume of macaque LGN (65-70 mm3) (Ahmad and Spear 1993; Malpeli et al. 1996). These values are consistent with estimates of the overall dimensions of the LGN: macaque, 3.75 mm (anteroposterior) × 4.9 mm (mediolateral) × 4.8 mm (dorsoventral) by Le Gros Clark (1941; see also Connolly and van Essen 1984) and marmoset 3.0 mm (anteroposterior) × 2.9 mm (mediolateral) × 2.8 mm (dorsoventral) (our data; see also Kaas et al. 1978; Spatz 1978). The total LGN volume in macaque is 88.2 mm3, and in marmoset the total LGN volume is 24.6 mm3. The ratio of these volumes is 3.6:1.
View this table:
TABLE 1.
LGN volume and visual field representation
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FIG. 8.
A: distribution of ML opponent responses in the PC layers (PC) and interlaminar zone (IPM). Each point shows the relative response amplitude for luminance (LUM) and red-green chromatic (RG) stimuli as a function of cell position relative to the borders of the internal or external PC lamina. Open circles, trichromats; closed circles, dichromats. RG opponent cells in trichromats are distributed throughout the PC layers. In the interlaminar zone, both blue-ON (B-ON) and other cells (N-op) show relatively poor responses to RG modulation. B: data from PC cells are plotted as a function of receptive field eccentricity. Nearly all the cells that show RG opponent response have receptive fields located 
10° of the fovea.
; Kaplan and Shapley 1986; Schiller and Malpeli 1978; Wiesel and Hubel 1966). There is also a segregation within the PC laminae, so that ON-center cells are more frequently encountered in the external part of each PC layer and OFF responses predominate in the internal one-half of each layer. The difference between the internal and external one-half of each layer is statistically significant for the PC layers (Mann-Whitney U = 3127.5, P = 0.0048). No such segregation is apparent for the magnocellular layers (Mann-Whitney U = 159.5, P = 1) nor was a clear difference apparent for dichromatic or trichromatic animals.
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FIG. 6.
Distribution of ON and OFF responses within the PC and MC layers. A: peristimulus time histograms of the response of 1 ON cell and 1 OFF cell to sinusoidal luminance (in-phase) modulation of red and green LEDs at 3.906 Hz. B: schematic outline of 1 LGN lamina. Location of each cell (open circles) in a given electrode track (vertical line) was measured with respect to the laminar borders (gray lines). C and D: histograms to show the number of ON and OFF cells encountered within 25% depth ranges within the PC (C) and MC (D) laminae.
; in both macaque and marmoset, MC cells have a steeper contrast-response relationship than PC cells, and response saturation is evident at high contrast levels for MC cells. (Blakemore and Vital-Durand 1986; Derrington and Lennie 1984; Hicks et al. 1983; Kaplan and Shapley 1986).
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FIG. 7.
Responses of different cell types in the LGN to contrast varying stimuli modulated at 3.906 Hz. Each row shows the responses of a different cell to two different stimulus paradigms; in-phase (LUM, A) or out of phase (RG, B) modulation of luminance matched red and green LEDs. The stimulus contrast was modulated with a sine wave envelope over a 4.1-s epoch. Average peristimulus histograms for 16 stimulus presentations are shown. Vertical scale 20 impulses/s. C: amplitude of the 3.906-Hz Fourier component of the cell's response for each stimulus is compared. The significant response to chromatic modulation defines the opponent PC cell. The MC cell shows greater achromatic contrast sensitivity than the PC cell.
, who showed a high proportion of nonopponent cells in trichromatic females. This result is different from the situation in macaque, in which the vast majority of PC cells show cone opponency when tested with appropriate stimuli (De Monasterio et al. 1975; Derrington et al. 1984; Padmos and Van Norren 1975).
). In trichromatic animals, it can also be attributed to the nonlinearity of cone summation in MC projecting cells (Lee et al. 1989a; Yeh et al. 1995b). The MC cells will not be considered further here.
) as for macaque (Derrington et al. 1984; Dreher et al. 1976; Wiesel and Hubel 1966) ML opponent responses are restricted to the PC layers of the LGN.
reported the presence of cells receiving input from SWS cones in marmoset LGN but did not characterize these cells further. In this study a small number of cells (n = 13) was identified as blue-ON by their responses to handheld stimuli. As for blue-ON cells in macaque LGN (Derrington et al. 1984) and retina (Lee et al. 1989b; Yeh et al. 1995b), these cells are sensitive to stimuli designed to modulate, selectively, the SWS cones (Fig. 9A). The response to in-phase modulation of the red and green diodes (Fig. 9B) is of comparable amplitude and opposite phase to the response to SWS cone modulation (Fig. 9, C-E). Responses to the SWS isolating stimulus were not seen in nonopponent PC cells (Fig. 9F), other interlaminar zone cells (Fig. 9G), or ML opponent PC cells (data not shown). The majority of MC cells showed no response (Fig. 9H). Some MC cells with very high sensitivity to luminance contrast did show some response to SWS modulation, but it is likely to be due to a residual luminance component in the stimulus because, for ON-center cells, the response to SWS modulation had the same phase as the response to luminance modulation.
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FIG. 9.
Responses of cells to short-wavelength sensitive (SWS) isolating stimulus. A and B: blue-ON cell. The stimulus waveform is sketched above peristimulus time histograms for (A) in-phase modulation of red and green LEDs (LUM) and (B) SWS cone isolating stimulus. Vertical scale, 10 impulses/sec. C and D: amplitude (C) and phase (D) of the 3.906-Hz Fourier component of the cell response to each stimulus. The cell shows contrast-dependent responses to both stimuli at opposite phase to SWS (blue-ON) and LUM (yellow-OFF). E-G: responses of other cells to these stimuli. Amplitude values shown as in C. Blue-ON cells (E) always respond to the SWS stimulus, but there is no response to the SWS stimulus for the majority of nonopponent (F) PC cells, of interlaminar zone (G) cells. MC cells (H) respond vigorously to luminance contrast but show little or no response to SWS modulation.
that blue-ON cells are segregated to the interlaminar zones, by showing that ML responses are likewise segregated, but the segregation is to the main PC layers.
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FIG. 10.
A: outline drawings of coronal sections at 4 levels through the posterior one-half of the marmoset LGN, showing the location of blue-ON cells ( 
) and ML opponent cells (
). Results pooled from 4 animals. The majority of blue-ON cells is located in the interlaminar zone between the MC and PC laminae. B: comparison of the intralaminar location of blue-ON cells with ML opponent cells. The location of each recorded cell with respect to the laminar borders is shown as a histogram. Blue-ON cells are segregated to the interlaminar zones and the internal border of the internal PC layer, but ML opponent responses are distributed throughout the PC layers. Abbreviations as for Fig. 1.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
; Malpeli and Baker 1975; Malpeli et al. 1996). Two other shared features are apparent. First, in both species the ratio of PC to MC volume is similar (marmoset, 3:1; macaque, 4.1:1, Table 1). Second, the PC:MC ratio is slightly higher in the central 5° than outside. Our results cannot address directly the controversial issue of whether the ratio of PC to MC cells decreases with eccentricity (Ahmad and Spear 1993; Connolly and van Essen 1984; Livingstone and Hubel 1988; Malpeli et al. 1996; Schein and De Monasterio 1987), but we note (Table 1) that the marmoset LGN does not show the kind of decrease calculated for macaque (Connolly and Van Essen 1984; Malpeli et al. 1996).
; Walls 1953; Wilder et al. 1996), but it is not evident in afoveate primates (reviewed by Casagrande and Norton 1991). Ganglion cell density and foveal cone topography are similar in macaque and marmoset (Schein 1988; Troilo et al. 1993; Wässle et al. 1989; Wilder et al. 1996), suggesting that the large volume of LGN devoted to the fovea serves to allow precise connectivity between retinal ganglion cells and geniculocortical relay cells (Conley and Fitzpatrick 1989; Spear et al. 1996; Walls 1953). This is all consistent with the hypothesis that the presence of a fovea is a necessary condition for trichromacy in primates. Accordingly, all the afoveate primate species whose color vision was studied are either dichromats or monochromats (reviewed by Jacobs 1993).
; Kaplan and Shapley 1986; Schiller and Colby 1983; Schiller and Malpeli 1978; Wiesel and Hubel 1966). This finding can be reconciled with our results if one accepts that the two internal PC layers in macaque are each functionally equivalent to the internal aspect of one PC layer in marmoset. Furthermore, a parallel can be drawn with other mammals in which there is a clear segregation of ON and OFF responses within the LGN [mink (Le Vay and McConnell 1982), ferret (Stryker and Zahs 1983), and tree shrew (Conway and Schiller 1983; Holdefer and Norton 1995)]. For all these species, as for primates, the ON responses are segregated furthest from the optic tract for each eye's territory in the LGN. This segregation is independent of the chromatic phenotype of the animal.
16° of the fovea. Although our sample of ML opponent cells is small, the results are consistent with the hypothesis that the generation of ML opponent responses depends on the precise connectivity among cones, midget bipolar cells, and midget ganglion cells, which is specific to the central retina in primates.
; this study) was unexpected given that similar (large field; low spatial frequency dominated) stimuli reveal opponent behavior in the majority of PC pathway cells in macaque retina and LGN (De Monasterio et al. 1975; Derrington et al. 1984; Padmos and Van Norren 1975). The low proportion of ML opponent cells in marmoset could arise because the density of cones in the perifoveal retina of marmoset is higher than that for macaque (Goodchild et al. 1996). For example, between 10 and 15° from the fovea, the numerical convergence of cones to midget cells for macaque is <5:1 but for marmoset is over 30:1 (Goodchild et al. 1996). Accordingly, mathematical simulations (De Valois and De Valois 1993; Lennie et al. 1991; Paulus and Kröger-Paulus 1983) show that the proportion of ML opponent cells should decrease with increasing convergence if the opponent cells draw their input indiscriminately from the local ML cone array. Recent in vitro studies of midget ganglion cells in the far peripheral retina in macaque (Dacey 1994; Dacey and Lee 1997) likewise show that reduced ML opponency is present where cone convergence is greater.
; Casagrande and Norton 1991). Our finding that SWS opponent signals are segregated to the interlaminar zone (Martin et al. 1997; this study) is likewise consistent with recent evidence that blue-ON responses are segregated to the interlaminar zones in the macaque (Reid et al. 1997) and add to the evidence for a distinct pathway for SWS cone signals within the retina (Dacey and Lee 1994; Ghosh et al. 1997; Kouyama and Marshak 1992) and central visual pathways of primates. Our results suggest that only a small proportion of interlaminar zone cells are blue-ON cells, but we did not study systematically the properties of the other (nonopponent) cell types, except to confirm that the visuotopic map in the interlaminar zone is in broad register with that of the main PC and MC layers. Nevertheless, our qualitative assessment of the receptive fields of interlaminar zone cells clearly indicated that, as for koniocellular cells in the nocturnal prosimian Galago (Norton and Casagrande 1982), the interlaminar zone cells in marmoset show a wide variety of response properties. More recent anatomic data likewise suggest that there may be morphological and neurochemical heterogeneity in the koniocellular pathway in Galago (Ding and Casagrande 1997) and marmoset (Goodchild and Martin 1998). That the interlaminar/koniocellular division of the LGN in marmoset is anatomically segregated from the PC layers enabled the blue-ON cells to be assigned with confidence to the koniocellular pathway in this study and give promise that other functional subgroups of cells in the "third geniculocortical pathway" (Casagrande 1994; Hendry and Yoshioka 1994) can be delineated in this species.
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ACKNOWLEDGEMENTS |
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We thank R. Phillips and A. Lara for technical assistance and J. Potas for assistance with the LGN reconstructions; J. Kremers, T. Yeh, B. B. Lee, and U. Grünert for helpful comments and discussion; and Dr. Sander Beckers and Abbot Australasia for the kind donation of isofluorane used in these experiments.
This work was supported by National Health and Medical Research Council of Australia Grant 096070.
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FOOTNOTES |
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Address for reprint requests: P. R. Martin, Dept. Physiology F13, University of Sydney, NSW 2006, Australia.
Received 5 January 1998; accepted in final form 1 July 1998.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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 J. D. Crook, B. B. Peterson, O. S. Packer, F. R. Robinson, P. D. Gamlin, J. B. Troy, and D. M. Dacey The Smooth Monostratified Ganglion Cell: Evidence for Spatial Diversity in the Y-Cell Pathway to the Lateral Geniculate Nucleus and Superior Colliculus in the Macaque Monkey J. Neurosci., November 26, 2008; 28(48): 12654 - 12671. [Abstract] [Full Text] [PDF]
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C. Tailby, S. G. Solomon, and P. Lennie Functional Asymmetries in Visual Pathways Carrying S-Cone Signals in Macaque J. Neurosci., April 9, 2008; 28(15): 4078 - 4087. [Abstract] [Full Text] [PDF]
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 V. Casagrande, F Yazar, K. Jones, and Y Ding The Morphology of the Koniocellular Axon Pathway in the Macaque Monkey Cereb Cortex, October 1, 2007; 17(10): 2334 - 2345. [Abstract] [Full Text] [PDF]
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 B. A. Szmajda, P. Buzas, T. FitzGibbon, and P. R. Martin Geniculocortical relay of blue-off signals in the primate visual system PNAS, December 19, 2006; 103(51): 19512 - 19517. [Abstract] [Full Text] [PDF]
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P. Buzas, E. M. Blessing, B. A. Szmajda, and P. R. Martin Specificity of M and L Cone Inputs to Receptive Fields in the Parvocellular Pathway: Random Wiring with Functional Bias J. Neurosci., October 25, 2006; 26(43): 11148 - 11161. [Abstract] [Full Text] [PDF]
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P. R. Jusuf, P. R. Martin, and U. Grunert Random Wiring in the Midget Pathway of Primate Retina J. Neurosci., April 12, 2006; 26(15): 3908 - 3917. [Abstract] [Full Text] [PDF]
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E. M Callaway Structure and function of parallel pathways in the primate early visual system J. Physiol., July 1, 2005; 566(1): 13 - 19. [Abstract] [Full Text] [PDF]
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E. M. Blessing, S. G. Solomon, M. Hashemi-Nezhad, B. J. Morris, and P. R. Martin Chromatic and spatial properties of parvocellular cells in the lateral geniculate nucleus of the marmoset (Callithrix jacchus) J. Physiol., May 15, 2004; 557(1): 229 - 245. [Abstract] [Full Text] [PDF]
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 J. A. Landers, I. Goldberg, and S. L. Graham Detection of Early Visual Field Loss in Glaucoma Using Frequency-Doubling Perimetry and Short-Wavelength Automated Perimetry Arch Ophthalmol, December 1, 2003; 121(12): 1705 - 1710. [Abstract] [Full Text] [PDF]
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 D. J. McKeefry, N. R. A. Parry, and I. J. Murray Simple Reaction Times in Color Space: The Influence of Chromaticity, Contrast, and Cone Opponency Invest. Ophthalmol. Vis. Sci., May 1, 2003; 44(5): 2267 - 2276. [Abstract] [Full Text] [PDF]
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Y. Shostak, Y. Ding, J. Mavity-Hudson, and V. A. Casagrande Cortical Synaptic Arrangements of the Third Visual Pathway in Three Primate Species: Macaca mulatta, Saimiri sciureus, and Aotus trivirgatus J. Neurosci., April 1, 2002; 22(7): 2885 - 2893. [Abstract] [Full Text] [PDF]
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S. G. Solomon, A. J. R. White, and P. R. Martin Extraclassical Receptive Field Properties of Parvocellular, Magnocellular, and Koniocellular Cells in the Primate Lateral Geniculate Nucleus J. Neurosci., January 1, 2002; 22(1): 338 - 349. [Abstract] [Full Text] [PDF]
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A. J R White, S. G Solomon, and P. R Martin Spatial properties of koniocellular cells in the lateral geniculate nucleus of the marmoset Callithrix jacchus J. Physiol., June 1, 2001; 533(2): 519 - 535. [Abstract] [Full Text] [PDF]
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X. Xu, J. M Ichida, J. D Allison, J. D Boyd, A B Bonds, and V. A Casagrande A comparison of koniocellular, magnocellular and parvocellular receptive field properties in the lateral geniculate nucleus of the owl monkey (Aotus trivirgatus) J. Physiol., February 15, 2001; 531(1): 203 - 218. [Abstract] [Full Text] [PDF]
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B. B Lee, L. C. L Silveira, E. S Yamada, D. M Hunt, J. Kremers, P. R Martin, J. B Troy, and M. da Silva-Filho Visual responses of ganglion cells of a New-World primate, the capuchin monkey, Cebus apella J. Physiol., November 1, 2000; 528(3): 573 - 590. [Abstract] [Full Text] [PDF]
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J. D. Boyd, J. A. Mavity-Hudson, and V. A. Casagrande The Connections of Layer 4 Subdivisions in the Primary Visual Cortex (V1) of the Owl Monkey Cereb Cortex, July 1, 2000; 10(7): 644 - 662. [Abstract] [Full Text] [PDF]
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W M. Usrey and R C. Reid Visual physiology of the lateral geniculate nucleus in two species of New World monkey: Saimiri sciureus and Aotus trivirgatis J. Physiol., March 15, 2000; 523(3): 755 - 769. [Abstract] [Full Text] [PDF]
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Y. H. Yucel, Q. Zhang, N. Gupta, P. L. Kaufman, and R. N. Weinreb Loss of Neurons in Magnocellular and Parvocellular Layers of the Lateral Geniculate Nucleus in Glaucoma Arch Ophthalmol, March 1, 2000; 118(3): 378 - 384. [Abstract] [Full Text] [PDF]
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V. A Casagrande The mystery of the visual system K pathway J. Physiol., June 15, 1999; 517(3): 630 - 630. [Full Text] [PDF]
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S. G Solomon, A. J R White, and P. R Martin Temporal contrast sensitivity in the lateral geniculate nucleus of a New World monkey, the marmoset Callithrix jacchus J. Physiol., June 15, 1999; 517(3): 907 - 917. [Abstract] [Full Text] [PDF]
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