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REPORT
Visual Sciences, Research School of Biological Sciences, Australian National University, Canberra, ACT, Australia
Submitted 9 November 2004; accepted in final form 15 January 2005
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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first categorized cells in the primary visual cortices of cats into two distinct cell types: simple and complex. The distinction was based on the spiking responses of cells during four visual tests. Simple cells 1) have spatially segregated ON and OFF regions within their receptive fields; 2) show summation within each subregion; 3) have antagonistic ON and OFF subregions; and 4) have responses that can be predicted based on the organization of their receptive field (RF) subregions. Cells that did not meet all or any of these criteria were classified as complex. Since the pioneering observations of Hubel and Weisel, a method was developed to quantify the simple and complex categories based on the spiking responses of the cells to moving sinusoidal gratings ( De Valois et al. 1982; Movshon et al. 1978a, b; for review, Skottun et al. 1991). The method calculates the mean response of the cells above spontaneous rate during the period of motion (F0) and the amplitude of oscillations at the fundamental temporal frequency of the stimulus (F1). An F1/F0 ratio is then calculated. Skottun et al. (1991) showed that, when the ratios were plotted for a large population of cells in cat and monkey V1, the neurons fell into a bimodal distribution with peaks at ratios of 1.7 and 0.2–0.3. There was a clear minimum or dip close to an F1/F0 ratio of unity. Separating the neuron types based on those with F1/F0 ratios >1 or <1 produced a distribution that correlated well with the classifications based on the qualitative measures suggested by Hubel and Weisel (1962). Cells with ratios below unity were classed as complex cells and the others as simple cells.
We know that mammals originated from reptile-like therians in the cretaceous period (e.g., Ibbotson and Mark 2003; Mark and Marotte 1992). Approximately 135 million years ago, the therians split into two major radiations: the metatherians (marsupials) and eutherians (placentals). The majority of what we know about cortical physiology is based on recordings from eutherians (primarily cats and monkeys). Using qualitative methods, cells with simple and complex-like properties have been reported in two nocturnal marsupials: an American opossum, Didelphis aurita ( Rocha-Miranda et al. 1976), and an Australian possum, Trichosaurus vulpecula ( Crewther et al. 1984). Simple and complex cells have also been identified qualitatively in a highly visual, day-and-night active marsupial, the Tammar wallaby, Macropus eugenii ( Ibbotson and Mark 2003; Vidyasagar et al. 1992). These studies showed that cortical neurons in the wallaby are highly tuned for orientation, spatial, and temporal frequency in much the same way as cortical cells in rats, cats, and monkeys (e.g., Girman et al. 1999). Given that the two main mammalian radiations split so long ago, it is of interest to further compare the physiology of the marsupial primary visual cortex with eutherian mammals in more detail. Here we provide the first quantitative evidence for the existence of simple and complex cells at the extracellular level in the cortex of the Tammar wallaby and compare the data with that from the cat.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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). Briefly, animals were anesthetized using intravenous infusion of 1 mg/kg/h of pentobarbital sodium (Boehringer-Ingleheim), paralyzed using suxamethonium chloride (4.2 mg/kg/h; Glaxo), and artificially respired with oxygen and N2O. After extracellular isolation of individual units in primary visual cortex (area 17), direction tuning and locations of ON and OFF regions were qualitatively tested using hand-driven light bars. Optimal direction, spatial frequency, temporal frequency, and classical receptive field size were determined quantitatively with computer-driven monochromatic sinusoidal gratings (frame rate, 100 Hz; mean luminance, 45 cd/m2). F1/F0 ratios were calculated from gratings with contrasts >32% moving in the neuron's preferred direction, spatial frequency, and temporal frequency. Test gratings were presented for 6 s in most cases (8–32 repeats), interleaved with a uniform gray of mean luminance for 10 s. In a proportion of cells that were lost before completing all tests, F1/F0 ratios were calculated using data from the initial spatial/temporal frequency tests, which were 2 s in duration. These data were only used if the optimum temporal frequency (TF) was 
2 Hz, thus giving several full response cycles to calculate the F1/F0 ratio. The F1 component of the response was calculated using Fourier analysis. The first cycle of each response was excluded from the analysis to prevent onset transients influencing either the F1 or F0 components. Spontaneous activity was subtracted from responses before calculation of the F1 or F0 components. All procedures were approved by the animal ethics committee of the Australian National University. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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, as well as previously unpublished data. All neurons used in this analysis showed orientation or direction tuning, and there was no systematic relationship between orientation tuning and F1/F0 ratio. Nondirectional cells were excluded from the data set, and all ratios were calculated using responses elicited by motion in the preferred direction. Figure 1 shows responses from two neurons in the primary visual cortex of the wallaby when stimulated by optimally oriented sine-wave gratings drifting in the preferred direction. The neuron in Fig. 1A was highly orientation-tuned and direction-selective (see inset). It shows a highly oscillatory response waveform at the same frequency as the grating drift rate (1.22 Hz) during preferred direction motion. This cell was classed as a simple cell using both the F1/F0 ratio and more traditional tests using hand-driven light bars. During preferred direction motion, the neuron in Fig. 1B shows no obvious oscillations at the fundamental stimulus frequency (3.1 Hz), but instead, has a large steady spiking output. This cell was classified quantitatively and qualitatively as a complex cell. It showed clear orientation tuning but was approximately equally responsive to motion in either direction along it preferred motion axis (Fig. 1B, inset).
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). The same cluster analysis was used to divide this population into two groups. Because we did not have access to the raw F1/F0 ratios, the cluster analysis was conducted by uniformly distributing the F1/F0 ratios for the cells in each column between the values at the extreme of each column. The dividing line between the populations for the cumulative cat data occurs at an F1/F0 ratio of 1.2.
Hartigan's dip statistic ( Hartigan and Hartigan 1985) revealed that the distributions of F1/F0 ratios in both wallaby and cat are significantly different from unimodality (P < 0.05). Using the same test separately on the simple and complex cell populations shows unimodal distributions (P > 0.8), revealing that, as a whole, both populations are bimodal. Wilcoxon rank-sum tests showed a difference of P < 0.03 between the medians of the cat and wallaby simple cells and P < 0.06 between the medians of the cat and wallaby complex cells. Wilcoxon rank-sum tests showed highly significant differences (P << 0.01) when simple and complex medians were compared.
The wallaby cortex does not have large sulci ( Vidyasagar et al. 1992), so penetrations were typically perpendicular to the cell layers, thus ensuring that the electrode traveled through all layers (Fig. 3A). Complex cells were reasonably evenly distributed throughout the cortical layers, whereas simple cells were more common in layers 4–6 (Fig. 3B).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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). Our results show that neurons in the primary visual cortex of the marsupial Tammar wallaby can also be classified as simple or complex cells based on F1/F0 ratios. The dips between simple and complex populations in rat ( Girman et al. 1999), cat, monkey, and wallaby are all close to unity. The quantitative findings from the wallaby confirm earlier qualitative reports that its cortical cells can be divided into those with or without distinct ON and OFF zones in their receptive fields ( Ibbotson and Mark 2003; Vidyasagar et al. 1992). Based on this data, we are confident that neurons in the wallaby cortex can be divided into simple and complex types.
Many have considered the bimodal distribution of the F1/F0 ratio as an indication of two different mechanisms at work in the cortex (for reviews, Mechler and Ringach 2002; Skottun et al. 1991). However, Mechler and Ringach (2002) showed through modeling that the underlying membrane potential modulation can be similar in simple and complex cells and that it is only the nonlinear spike-generating mechanism that leads to a bimodal F1/F0 ratio. The V1/V0 ratio is the intracellular equivalent of the F1/F0 ratio, with V0 being the mean depolarization of the membrane potential from the cell's resting potential and V1 being the modulation in the membrane potential. Intracellular recordings from the cat cortex have revealed that the underlying membrane oscillations produce V1/V0 ratios with a unimodal distribution peaking around 0.1, whereas the F1/F0 ratios have a bimodal distribution peaking at 0.3 and 1.7 ( Priebe et al. 2004). These results imply that the nonlinear spiking mechanism contributes significantly to the generation of simple and complex categories. Importantly, the spiking component of the cortical cell responses is essential from a functional standpoint because only the information contained in the spike trains is transmitted along the axon to higher-order visual areas ( Abbott and Chance 2002). It is common for the response patterns derived from the spiking output of cells to be quite different from the intracellular membrane activity. For example, the orientation tuning functions of neurons in cat cortex are wider when measured using membrane potential fluctuations instead of spiking responses ( Carandini and Ferster 2000).
Further support that the same basic cortical circuit generates simple and complex responses comes from experiments showing that cells in cat areas 17/18 can be converted from simple into complex by blocking the action of GABA, an inhibitory neurotransmitter ( Borg-Graham et al. 1998; Chance et al. 1999; Frégnac and Shulz 1999; Pernberg et al. 1998). It is conjectured that inhibitory interneurons normally hyperpolarize simple cell membrane potentials well below spiking threshold. Removal of the inhibition depolarizes the resting membrane potential, thus making it easier for the cell to spike. Kagan et al. (2002) have shown that there are fewer simple cells in awake behaving monkeys than in anesthetized animals, perhaps indicating state-dependent modulation of cortical circuitry.
Similarities in the anatomical connections of the geniculostriate pathways in monkeys, cats, and wallabies suggest that the cortical circuitry has a common design (e.g., Henry and Mark 1992; Mark and Marotte 1992; Sheng et al. 1990, 1991; Tyler et al. 1998; Vidyasagar et al. 1992; Wimborne et al. 1999). Given this similarity, the presence of simple and complex cells in wallaby might be expected. Furthermore, due to general similarities in the connectivity of the geniculo-striate pathway in mammals, between-species variations in visual response properties may be based more on visual ecology than phylogenetic distance between species ( Ibbotson and Mark 2003). For example, both cats and wallabies are day and night active species with good spatial acuity ( Hemmi and Mark 1998) and have been shown here to have similar F1/F0 ratios. However, visual ecology is unlikely to be the only determining factor of F1/F0 ratios, because the rat, which is not regarded as a highly visual animal, also has a similar F1/F0 distribution ( Girman et al. 1999). It is a goal for future comparative studies to find if bimodal F1/F0 distributions occur in all visual mammals or only those with highly orientation selective visual cortices. Our findings add to the argument of Mark and Marotte (1992) that the wallaby is a valid animal model to study vision, but with the added benefit that early development can be studied more easily due to slow embryonic development and access to developing pouch young. The comparative use of the wallaby is now further reinforced by the recent initiation of the kangaroo genome project, of which the wallaby forms the experimental model ( Wakefield and Graves 2003).
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GRANTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: M. R. Ibbotson, Visual Sciences, Research School of Biological Sciences, Australian National Univ., Canberra, ACT 2601, Australia (E-mail: Michael.Ibbotson{at}anu.edu.au)
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REFERENCES |
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