Research Articles
Activity correlates of cytochrome oxidase-defined compartments in granular and supragranular layers of primary visual cortex of the macaque monkey
- Edgar A. Deyoe, Thomas C. Trusk, Margaret T.T. Wong-Riley
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- Published online by Cambridge University Press:
- 02 June 2009, pp. 629-639
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To determine if changes in metabolic capacity revealed by cytochrome oxidase (CO) histochemistry are related to sustained changes in energy-utilizing neuronal activity, we assayed CO levels and recorded multiunit firing rates along nearly tangential penetrations of V1 in seven adult macaque monkeys before and after single, monocular injections of TTX. Within as little as 14 h, TTX blockade began to reduce CO staining in zones of layer 4C that received dominant input from the injected eye. Since simple monocular occlusion has only minor effects on cortical CO levels (Trusk et al., 1990), the changes in activity that were specifically associated with CO depletion were isolated by comparing spike rates during monocular TTX blockade and during monocular occlusion. Five second samples of multiunit spike rate were obtained after 2-min adaptation to each of four adapting fields: black, gray, white, and textured. Results were similar for these four conditions. In layer 4C, ocular dominance zones with input from the TTX eye had ongoing spike rates that were 48% of the rates in zones with input from a normal but occluded eye. In six animals, it was possible to record activity at a single site before, during, and after the onset of TTX blockade. Background activity at these interpuff sites decreased as much as 3-fold in less than 1 h but stabilized within 3–4 h to an average of 53% of pre-TTX rates. These data support the interpretation that energy utilization linked to sustained spike rates partially regulates CO levels under normal conditions, at least in layer 4. Furthermore, changes in neuronal activity induced by retinal TTX preceded the detectable reduction in CO activity in V1 suggesting that the adjustment of CO levels was in response to the altered activity.
Neuronal activity in primate visual cortex assessed by immunostaining for the transcription factor Zif268
- Avi Chaudhuri, Joanne A. Matsubara, Max S. Cynader
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- 02 June 2009, pp. 35-50
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It is now well established that environmental signals mediated via neurotransmitters and hormones can induce responses in cells which involve a cascade of receptors, G proteins, and second messengers. These in turn can induce transcription factors which regulate long-term changes in gene expression. It has been proposed that the stimulus-transcription coupling properties of these DNA-binding proteins can be exploited to visualize activated neurons by way of immunostaining. We have used standard immunohistochemical techniques to detect the expression of one specific transcription factor, Zif268, in the visual cortex (area 17, V1) of vervet monkeys (Cercopithecus aethiops). Immunopositive neurons were present in large numbers throughout the visual cortex of the normal animal, being concentrated in layers 2/3 and 6 and at moderate levels in 4Cβ and 5. To determine if Zif268 expression was affected by visual stimulation in the monkey, we restricted light input to one eye with the aim of revealing ocular-dominance columns in striate cortex. We found that short-term monocular deprivation induced either by enucleation, intravitreal TTX injection, or eyelid suturing resulted in dramatic changes in Zif268 levels, revealing vertically oriented columns of reduced Zif268 staining interdigitated with columns of normal expression. Furthermore, these columns were discernible after just 2 h of monocular blockade. A comparison of the ocular-dominance pattern obtained with Zif268 immunostaining and cytochrome oxidase histochemistry in long-term monocularly deprived animals showed a coincident reduction of both markers along columns that were precisely aligned in adjacent sections, indicating that Zif268 expression is restricted to cortical regions of high metabolic activity. Simultaneous immunostaining for Zif268 and the calcium-binding proteins calbindin and parvalbumin showed a negative correlation, suggesting that the Zif268 protein may be expressed selectively within excitatory neurons. A similar approach with immunostaining for neurofilament and microtubule-associated proteins (SMI-32 and MAP2) revealed pyramidal neurons which were regularly found to contain a Zif268-positive nucleus. Furthermore, confocal images of lucifer yellow filled neurons possessing Zif268-positive nuclei all showed pyramidal morphology. Taken together, these results point to activity-dependent expression of Zif268 within a subset of excitatory neurons.
The VEP thresholds for full-field stimuli in dark-adapted infants
- Ronald M. Hansen, Anne B. Fulton
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- Published online by Cambridge University Press:
- 02 June 2009, pp. 223-228
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Dark-adapted adults' electroretinographic b−wave thresholds are —2 log units below a−wave thresholds and ~3 log units above the perceptual threshold, and their perceptual and the visually evoked cortical potential (VEP) thresholds are similar. Dark-adapted infants' scotopic a− and b−wave thresholds for full-field stimuli are both about 0.5 log units above those of adults, but their scotopic VEP thresholds for such stimuli have not been studied. We obtained scotopic VEP thresholds for brief, full-field stimuli from dark-adapted, infants and adults to consider the relationships of the cortical responses to the responses of more distal structures, namely the rod photoreceptors (scotopic a−wave) and ON-bipolars (scotopic b−wave). The median VEP threshold of infants is 0.5 log unit above that of adults. Thus, the relationships of a− and b−wave and VEP thresholds in infants are similar to those in adults. These results are consistent with rod cell immaturities being the primary determinant of the difference between infants' and adults' thresholds.
Phototransduction: Modeling the primate cone flash response
- Russell D. Hamer, Christopher W. Tyler
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- 02 June 2009, pp. 1063-1082
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We have developed a new model of phototransduction that accounts for the dynamics of primate and human cone flash responses in both their linear and saturating range. The model incorporates many of the known elements of the phototransduction cascade in vertebrate photoreceptors. The input stage is a new analytic expression for the activation and inactivation of cGMP-phosphodiesterase (PDE). Although the Lamb and Pugh (1992) model (of a delayed ramp for the rising phase of the PDE* response in amphibian rods) provided a good fit for the first 2 log units of stimulus intensity without parameter adjustments, the remaining 4 log units of the data required nonlinear modifications of both delay and gain (slope). We show that this nonlinear behavior is a consequence of the delay approximation and develop a completely linear model to account for the rising phase of amphibian rod photocurrent responses over the full intensity range (~6 log units). We use the same dynamic model to account for primate cone responses by decreasing the time constants of PDE activation and introducing an enhanced inactivation process. This PDE* response activates a nonlinear calcium feedback stage that modulates guanylate cyclase synthesis of cyclic GMP. By adjustment of the throughput and feedback parameters, the full model successfully captures most of the features of the primate and human cone flash responses throughout their dynamic range. Our analysis suggests that initial processes in the transduction cascade may be qualitatively different from comparable processes in rods.
Response linearity and kinetics of the cat retina: The bipolar cell component of the dark-adapted electroretinogram
- J. G. Robson, L. J. Frishman
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- Published online by Cambridge University Press:
- 02 June 2009, pp. 837-850
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The electroretinogram (ERG) of the dark-adapted cat eye in response to brief ganzfeld flashes of a wide range of intensities was recorded after intravitreal injection of n-methyl dl aspartate (NMdlA, cumulative intravitreal concentration of 1.3–3.9 mM) to suppress inner-retinal components, and after intravitreal dl or L-2-amino-4-phosphonobutyric acid (dl-APB, 1–3 mM; l-APB, 1.2 mM) and 6-cyano-7-nitroquinoxaline-2, 3 dione (CNQX, 40–60 µM), to suppress all post-receptoral neuronal responses. Rod PII, the ERG component arising from rod bipolar cells, was derived by subtracting records obtained after APB and CNQX from post-NMDLA records. When we measured the derived response at fixed times after the stimulus, we found that PII initially increased in proportion to stimulus intensity without any sign of a threshold. The leading edge of PII at early times after the stimulus, when the response was still small, was well described by V(t) = kI(t −td)5 where k is a constant, I is the intensity of the stimulus, and td is a brief delay of about 3 ms. Correspondingly, the time for the response to rise to an arbitrary small criterion voltage Vcrit was adequately fitted by tcrit = td + (Vcrit/kI)1/5. The time course of the leading edge of the PII response can be interpreted to indicate that the mechanism generating PII introduces three stages of temporal integration in addition to the three stages that are provided by the mechanism of the rod photoreceptors. This finding is consistent with the operation within the rod bipolar cell of a G-protein cascade similar to that in the rods.
Effects of wavelength on the timing and laminar distribution of illuminance-evoked activity in macaque V1
- S.J. Givre, J.C. Arezzo, C.E. Schroeder
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- 02 June 2009, pp. 229-239
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Responses to full-field colored flashes (red, blue, and green) were compared with those to illuminancematched white flashes in area V1, optic radiations, and the lateral geniculate nucleus of two alert macaques. Laminar profiles of visual evoked potentials (VEPs), current source density, and multiunit activity were obtained using multicontact electrodes capable of sampling from all layers of cortex or lateral geniculate nucleus, simultaneously. In striate cortex, stimulation with colored flash enhanced transmembrane current flow dramatically in both layer 4c and the supragranular laminae. Stimulation with red evoked the largest enhancement in every electrode penetration. The mean peak amplitudes of current sinks evoked by red were 203% and 537% of those evoked by white light in layer 4c and the supragranular laminae, respectively. Color effects in VI were preceded by an initial epoch of wavelength-insensitive activity. In layer 4c, the red effect reached significance, on average, at 47 ms, or ≈24 ms after the onset of transmembrane current flow. In the supragranular layers, the red effect reached significance, on average, at 55 ms, or ≈14 ms after the onset of current flow. Recordings from optic radiations in the white matter below V1 and from lateral geniculate nucleus showed no significant difference in the responses to color and illuminance-matched white light. Enhancement of supragranular current flow with color stimulation increased the contribution of these laminae to the generation of the surface VHP. Comparison of the surface VHP wave forms evoked by white and color stimuli may, therefore, help to differentiate the responses of the granular and supragranular laminae.
Localization and expression of insulin-like growth factor in the teleost retina
- Andreas F. Mack, Steven L. Balt, Russell D. Fernald
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- Published online by Cambridge University Press:
- 02 June 2009, pp. 457-461
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Teleost fish retinas continue to add neurons throughout life, and evidence from in vitro experiments have implicated insulin-like growth factors (IGFs) in this process. To discover whether these factors are expressed in vivo, we have examined their expression in the cichlid fish, Haplochromis burtoni. Three lines of evidence show that IGFs are present in the fish retina. An IGF-I specific antibody, sm 1.2, binds preferentially to the retinal outer plexiform layer, in areas of cone photoreceptor synaptic endings. Northern blots of mRNA hybridized with riboprobes from trout IGF-I and IGF-II genes revealed transcripts of ~6.5 and 4.9 kb, respectively. The IGF-I probe detected an additional transcript of 1.2 kb in liver but not in retinal mRNA. In situ hybridization with digoxigenin-labeled riboprobes revealed that the IGF gene product is localized in the cone photoreceptors. These results show that cone photoreceptors are the source of IGFs in the fish retina, consistent with the hypothesis that IGFs play a role in regulating production of new neurons in the teleost retina.
Centrifugal innervation of the rat retina
- Michael Schütte
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- 02 June 2009, pp. 1083-1092
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Centrifugal fibers innervating the retina have been shown in all classes of vertebrate, except for mammals where conventional tract-tracing methods have not been able to unmistakably demonstrate their existence. In a previous study, a unilateral, intravitreal injection of 5, 7-dihydroxytryptamine was used to reveal indoleamine-accumulating centrifugal fibers which were visualized by an immunoreaction against serotonin. In the present study, I employed a modification of this method to stain retinopetal neurons in the rat. Terminals were located preferentially in the outer retina; labeled fibers could be traced back along an ipsilateral pathway to somata in the dorso-caudal portions of the chiasm or the medio-lateral preoptic area, and thence towards the suprachiasmatic nuclei. The unique beaded appearance of the fibers distinguishes them from retinal ganglion cell axons. The labeling of central cell bodies strongly suggests that they possess terminals in the retina. Thus, at least some mammalian retinas receive centrifugal innervation. This indoleamine-accumulating retinopetal pathway may be involved in retinal melatonin synthesis, coordination of circadian rhythms, and interocular phenomena.
Nerve growth factor preserves behavioral visual acuity in monocularly deprived kittens
- A. Fiorentini, N. Berardi, L. Maffei
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- 02 June 2009, pp. 51-55
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Recent electrophysiological and anatomical experiments in rats and cats have shown that treatment with the neurotrophic factor — nerve growth factor (NGF) — prevents the effects of monocular deprivation (MD) at the level of visual cortex and lateral geniculate nucleus. We tested whether NGF treatment was effective in preventing MD effects on visual behavior of monocularly deprived kittens. Behavioral visual acuity was measured in kittens that had been monocularly deprived and treated intraventricularly with NGF for 2 weeks during the critical postnatal period. The detrimental effects of MD on behavioral visual acuity were found to be largely prevented by NGF treatment.
Functional role of GABA in cat retina: I. Effects of GABAA agonists
- Thomas E. Frumkes, Ralph Nelson
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- 02 June 2009, pp. 641-650
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Putative GABAergic mechanisms were studied in perfused cat retina by means of intracellular recording and application of GABA and the GABAA agonists δ-amino valeric acid (dAVA), muscimol, and THIP. In contrast to results reported previously for cold-blooded vertebrates, introduction of 20 mM GABA into the superfusate had no influence upon the response properties of cat retinal horizontal cells (HCs). In common with results reported in cold-blooded vertebrates, introduction of the GABAA agonists dAVA (2–12 mM) and THIP or muscimol (0.2–1 mM) had four consistent reversible influences upon the response properties of cat retinal HCs: (1) they reduced photic-response amplitude, (2) slowed response onset, (3) slowed response offset, and (4) depolarized the dark membrane potential. Both rod and cone signal components were affected. GABAA agonists had similar influences upon both the time course and amplitude of responses recorded from amacrine and ganglion cells. In all cell types examined, the influence upon response kinetics was made particularly apparent with rapidly flickering stimuli. Flicker responses were reduced in amplitude much more than sustained responses. These results suggest that, in addition to other influences, GABAergic action serves to modify the time course of photic responses in both the inner and outer plexiform layer of mammalian retina making responses slower and less phasic.
The modulatory cholinergic system in goldfish tectum may be necessary for retinotopic sharpening
- John T. Schmidt
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- 02 June 2009, pp. 1093-1103
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The cholinergic circuit within the tectum and the cholinergic input from the nucleus isthmi mediate a presynaptic augmentation of retinotectal transmitter release via nicotinic receptors. In this study, the cholinergic systems were either eliminated using the cholinergic neurotoxin AF64A or blocked using nicotinic antagonists to test for effects on the activity-driven sharpening of the regenerating retinotectal projection. The effectiveness of the AF64A was verified by recording field potentials elicited by optic tract stimulation and by immunohistochemical staining for choline acetyltransferase (ChAT). At 1 week after intracranial (IC) injection of AF64A (12 to 144 nmoles) into the fluid above the tectum, field potentials showed a selective dose-dependent decrement of the cholinergic polysynaptic component with no effect on the amplitude of the glutamatergic monosynaptic component. The decrement was only partially recovered in recordings at 2 and 6 weeks. In normal fish, the ChAT antibody stains a population of periventricular neurons, their apical dendrites, and a dense plexus within the optic terminal lamina that consists of their local axons and fine dendrites and of input fibers from the nucleus isthmi. One week after IC AF64A injection (48–72 nmoles), most immunostaining in superficial tectum was lost but most neuronal somas in the deep tectum could still be seen, and staining in the tegmentum below the tectum was completely intact. At 2 weeks and later, the staining of neuronal somata largely recovered, but staining of the superficial plexus did not. AF64A treatment at 18 days after nerve crush, when regenerating retinal fibers are beginning to form synapses, prevented retinotopic sharpening of the projection. Recordings showed a rough retinotopic map on the tectum but the multiunit receptive fields (MURFs) at each tectal point averaged 34 deg vs. 11 deg in vehicle-injected control regenerates. AF64A treatment before nerve crush also blocked sharpening, ruling out a direct effect on retinal growth cones or retinal fibers, as AF64A rapidly decomposes, whereas its effect on the cholinergic fibers is long-lasting. IC injection or minipump infusion of the nicotinic antagonists α-bungarotoxin (αBTX), neuronal bungarotoxin (nBTX), and pancuronium during regeneration also prevented sharpening (MURFs averaging 29.4 deg, 33.0 deg, and 31.4 deg, respectively). Control Ringer≈s solution infusions or injections over the same period (19–37 days postcrush) had no effect on regenerated MURF size (11.7 deg). The results show that the cholinergic innervation, which modulates transmitter release, is required for activity-driven retinotopic sharpening, thought to be triggered by NMDA receptor activation.
Functional role of GABA in cat retina: II. Effects of GABAA antagonists
- Thomas E. Frumkes, Ralph Nelson, Renate Pflug
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- Published online by Cambridge University Press:
- 02 June 2009, pp. 651-661
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Putative GABAergic mechanisms were studied in the cat retina by exogenous application of the GABAA antagonists picrotoxin (PTX), native bicuculline (BCC), and bicuculline methyl bromide (BCC MeBr). When recording intracellular responses from horizontal cells (HCs) and amacrine cells as well as electroretinograms (ERGs), drugs were added to the perfusate used to maintain the isolated eyecup; when recording extracellular spikes from ganglion cells of anesthetized cats, drugs were introduced by iontophoretic injection. Both PTX and BCC MeBr had relatively little influence upon the response properties of HCs. In contrast, native BCC tended to decrease the amplitude of and to slow the photic response to light onset and both to quicken and to increase the amplitude of response to light offset; in the presence of native BCC, HC responses were dominated by a prominent spike-like “Off-overshoot.” The influence of GABAA agonists upon HC responses was not blocked by GABAA antagonists. ERG b−wave amplitude was reduced both by PTX and by native BCC, but was not influenced by BCC MeBr. Latency (time to half-peak) was increased by low doses of native BCC, and to a lesser extent PTX but not BCC MeBr. Rod-amacrine On-transient responses were increased in amplitude by PTX. Extracellular recordings from On- and Off- X and Y ganglion cell types became considerably more transient with application of either PTX, native BCC, or BCC MeBr; this tendency was greater in Off-type ganglion cells. Collectively, these results strengthen conclusions from the previous paper suggesting that GABA serves to slow onset and offset kinetics of retinal neurons, making them more sustained and less phasic. They also suggest that in mammalian retina heterogeneous types of GABAA receptors exist, segregated into different zones: a distal zone, sensitive only to native BCC, a central zone sensitive to both native BCC and PTX, and a proximal zone sensitive to native BCC, BCC methyl halides (BCC MeH), and PTX. Only the proximal zone obeys conventional GABAA pharmacology.
Organization of the hamster intergeniculate leaflet: NPY and ENK projections to the suprachiasmatic nucleus, intergeniculate leaflet and posterior limitans nucleus
- Lawrence P. Morin, J. Blanchard
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- 02 June 2009, pp. 57-67
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The intergeniculate leaflet (IGL) is an integral part of the circadian visual system. It receives direct retinal input and relays photic information to the circadian clock in the suprachiasmatic nucleus (SCN) through a geniculohypothalamic tract (GHT). In both rat and hamster, neuropeptide Y immunoreactive (NPY-IR) IGL cells project through the GHT to the SCN. However, the hamster GHT also contains enkephalin-IR (ENK-IR) fibers, presumably of IGL origin. In the present investigations, the IGL was examined for NPY-, ENK-, or dual-IR cells. Their projections to the SCN, contralateral IGL and pretectum were also studied. The results show that the hamster IGL contains both NPY- and ENK-IR neurons and that about 50% of these are immunoreactive to both peptides. Double-label retrograde analysis indicates that cells of each peptide class project to the SCN. Similarly, IGL neurons, many of which are NPY- and ENK-IR, project to the pretectum, particularly the posterior limitans nucleus. While numerous IGL neurons project contralaterally, very few are NPY- or ENK-IR.The distribution of SCN- and pretectum-projecting cells, in conjunction with the distribution of peptide-IR neurons, allows expansion of the IGL definition to include the region medial to the ventral lateral geniculate nucleus (VLG). The VLG is ventrolateral to the IGL and does not contain either neurons projecting to the SCN nor NPY- or ENK-IR cells, but does have numerous neurons projecting to the pretectum. The results substantiate and expand the previous definition of the hamster IGL, elaborate the species difference in IGL organization, and demonstrate the increased breadth of the circadian visual system.
Regional variations in the relative sensitivity to UV light in the mouse retina
- Jack B. Calderone, Gerald H. Jacobs
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- 02 June 2009, pp. 463-468
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About 3% of all mouse photoreceptors are cones. An earlier electrophysiological study indicated that there were two classes of cone in the mouse retina having peak sensitivities (λmax) of about 360 nm and 511 nm. Recent immunocytochemical results show there are two types of cones that have distinctive regional segregation patterns. We used regional stimulation of the retina in conjunction with electroretinogram (ERG) flicker photometry to see if the two cone types identified electrophysiologically are regionalized in a fashion suggested by the anatomical results. We find they are. Relative sensitivity to ultraviolet and visible light stimulation qualitatively parallels that predicted by immunocytochemical labelling. One result of this remarkable regionalization of cone types is that the mouse retina is relatively more sensitive to ultraviolet light stimulation when that light is directed toward the ventral half of the retina.
Simulation of the Aii amacrine cell of mammalian retina: Functional consequences of electrical coupling and regenerative membrane properties
- Robert G. Smith, Noga Vardi
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- 02 June 2009, pp. 851-860
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The Aii amacrine cell of mammalian retina collects signals from several hundred rods and is hypothesized to transmit quantal “single-photon” signals at scotopic (starlight) intensities. One problem for this theory is that the quantal signal from one rod when summed with noise from neighboring rods would be lost if some mechanism did not exist for removing the noise. Several features of the Aii might together accomplish such a noise removal operation: The Aii is interconnected into a syncytial network by gap junctions, suggesting a noise-averaging function, and a quantal signal from one rod appears in five Aii cells due to anatomical divergence. Furthermore, the Aii contains voltage-gated Na+ and K+ channels and fires slow action potentials in vitro, suggesting that it could selectively amplify quantal photon signals embedded in uncorrelated noise. To test this hypothesis, we simulated a square array of AII somas (Rm = 25,000 Ohm-cm2) interconnected by gap junctions using a compartmental model. Simulated noisy inputs to the Aii produced noise (3.5 mV) uncorrelated between adjacent cells, and a gap junction conductance of 200 pS reduced the noise by a factor of 2.5, consistent with theory. Voltage-gated Na+ and K+ channels (Na+: 4 nS, K+: 0.4 nS) produced slow action potentials similar to those found in vitro in the presence of noise. For a narrow range of Na+ and coupling conductance, quantal photon events (-5–10 mV) were amplified nonlinearly by subthreshold regenerative events in the presence of noise. A lower coupling conductance produced spurious action potentials, and a greater conductance reduced amplification. Since the presence of noise in the weakly coupled circuit readily initiates action potentials that tend to spread throughout the AII network, we speculate that this tendency might be controlled in a negative feedback loop by up-modulating coupling or other synaptic conductances in response to spiking activity.
The development of MK-801, kainate, AMPA, and muscimol binding sites in cat visual cortex
- Barbara Gordon, Ying L. Tseng, Rose Jaeger, Alexandra Petrovic, Kenneth Tovar
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- 02 June 2009, pp. 241-252
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Previous work using homogenate binding has shown that the development of (+)-5-methyl-10, ll-dihydro-5H-dibenzo[a, d]-cyclohepten-5, 10imine maleate (MK-801) binding in cat visual cortex increases from 21 days to 42 days, the height of the plastic period, and decreases in adulthood. We have studied the generality of this finding by examining the development of NMDA binding sites in several brain regions and by examining the development of other binding sites in the visual cortex. After confirming the original finding, we extended it by showing that the sensitivity of MK-801 binding sites to glutamate and glycine decreases when the cat becomes an adult. We then examined the regional specificity of MK-801 binding. Retinal binding did not change significantly with age. Binding in both visual cortex and hippocampus increased significantly from 7 days to 42 days regardless of whether binding was measured per milligram wet weight or per milligram protein. The decline from 42 days to adulthood was less dramatic in the hippocampus than in the visual cortex and was statistically significant only when binding was measured per milligram protein. Saturation analyses also showed a difference in the two structures. Bmax in the visual cortex, but not in the hippocampus, decreased from 42 days to adulthood. To determine whether these developmental changes were specific to MK-801 binding sites, we compared the age-dependent binding of MK-801, kainate, alpha-amino-3-hydroxy-5-methyl-4-isoxazoIepropionic acid (AMPA), and muscimol. Like MK-801, kainate binding increased from 7 days to 42 days and decreased from 42 days to adulthood. AMPA and muscimol binding showed a similar increase in binding from 7 days to 42 days but did not decrease significantly from 42 days to adulthood. Displacement experiments suggest that AMPA and kainate bind to separate sites. The 42-day peak in NMDA and kainate binding suggests that their associated receptors may have a role in determining the plastic period of visual cortex.
Fine structure analysis of temporal patterns in the light response of cells in the lateral geniculate nucleus of cat
- Florentin Wörgötter, Klaus Funke
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- 02 June 2009, pp. 469-484
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This study focuses on the analysis of temporal patterns in the spike train of cells in the lateral geniculate nucleus (LGN) of cat. Two-hundred eighty-three units have been recorded extracellularly in anesthetized animals during visual stimulation with flashing spot stimuli of different size. We used a novel method of temporally local computed interval distributions (intervalogram; Funke & Wörgötter, 1995) to visualize the statistical distribution of interspike intervals during different phases of the visual response. Multimodal interval distributions were observed mainly in X- and Y-ON cells, reflecting the tendency of these cells to fire with preferred intervals during the sustained light response. The shortest preferred interval is called the fundamental interval and the longer ones (higher-order intervals) are, in general, multiples thereof. During increasing surround inhibition a redistribution of the intervals towards the higher orders was observed. We regarded the different peaks in the interval distributions as different components of possible temporal spike sequences and performed a pattern search up to the level of five subsequent intervals. While it is obvious, that the dominant peak is most strongly represented in any interval sequence, we also show that a significant overrepresentation of short sequences of similar intervals exists. The repetition rate is rather small (4–5 intervals) and, therefore, no long-lasting oscillatory pattern was observed in the autocorrelograms. Power spectral analysis of the peristimulus-time histograms, however, revealed that the sequential firing pattern is strongly stimulus locked at least for the majority of sweeps in the records.
The mean firing rate of an LGN cell decreases with increasing stimulus size as well as with decreasing contrast. Therefore, the mean rate cannot be used to distinguish between these situations. While in the whole network this tradeoff can be resolved by the combined activity of multiple cells, our findings additionally suggest that contrast and size can be distinguished already at the single-cell level using different temporal patterns.
Tryptophan hydroxylase is expressed by photoreceptors in Xenopus laevis retina
- Carla B. Green, Gregory M. Cahill, Joseph C. Besharse
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- 02 June 2009, pp. 663-670
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Serotonin has important roles, both as a neurotransmitter and as a precursor for melatonin synthesis. In the vertebrate retina, the role and the localization of serotonin have been controversial. Studies examining serotonin immunoreactivity and uptake of radiolabeled serotonin have localized serotonin to inner retinal neurons, particularly populations of amacrine cells, and have proposed that these cells are the sites of serotonin synthesis. However, other reports identify other cells, such as bipolars and photoreceptors, as serotonergic neurons. Tryptophan hydroxylase (TPH), the rate-limiting enzyme in the serotonin synthetic pathway, was recently cloned from Xenopus laevis retina, providing a specific probe for localization of serotonin synthesis. Here we demonstrate that the majority of retinal mRNA encoding TPH is present in photoreceptor cells in Xenopus laevis retina. These cells also contain TPH enzyme activity. Therefore, in addition to being the site of melatonin synthesis, the photoreceptor cells also synthesize serotonin, providing a supply of the substrate needed for the production of melatonin.
Ultrastructural study of the optic nerve in blind mole-rats (Spalacidae, Spalax)
- M. Herbin, J.-P. Rio, J. RepéRant, H.M. Cooper, E. Nevo, M. Lemire
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- 02 June 2009, pp. 253-261
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The optic nerve in two species of subterranean mole-rats (Spalacidae) has been examined at the ultrastructural level. The axial length of the eye and the diameter of the optic nerve are 1.9 mm and 52.5 μm in Spalax leucodon, and 0.7 mm and 80.8 μm in Spalax ehrenbergi, respectively. An anti-glial fibrillary acidic protein postembedding procedure was used to distinguish glial cell processes from axons. In both species, the optic nerve is composed exclusively of unmyelinated axons and a spatial distribution gradient according to the size or the density of fibers is lacking. The optic nerve of S. leucodon contains 1790 fibers ranging in diameter from 0.07–2.30 μm (mean = 0.57 μm), whereas in S. ehrenbergi, only 928 fibers, with diameters of 0.04–1.77 μm (mean = 0.53 μm) are observed. In S. ehrenbergi, a higher proportion of glial tissue is present and the fascicular organization of optic fibers is less obvious. Distribution gradients according to size frequency or density of fibers in the optic nerve are absent in both species. Comparison with other mammals suggests that although ocular regression in microphthalmic species is correlated with a significant decrease in the total number of optic fibers and the relative proportion of myelinated fibers, no difference in the absolute size range of unmyelinated axons is observed. The total absence of myelinated fibers in Spalax may be related to the subcutaneous location of the eyes. The unique presence of unmyelinated fibers in the optic nerve is discussed in relation to the possible conservation of a single class of W-like ganglion cells in the retina, in relation to photoperiodic perception.
The morphology of the dorsal eye of the hydrothermal vent shrimp, Rimicaris exoculata
- Patrick J. O'Neill, Robert N. Jinks, Erik D. Herzog, Barbara-Anne Battelle, Leonard Kass, George H. Renninger, Steven C. Chamberlain
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- 02 June 2009, pp. 861-875
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The bresiliid shrimp, Rimicaris exoculata, lives in large masses on the sides of hydrothermal vent chimneys at two sites on the Mid-Atlantic Ridge. Although essentially no daylight penetrates to depths of 3500 m, very dim light is emitted from the hydrothermal vents themselves. To exploit this light, R. exoculata has evolved a modified compound eye on its dorsal surface that occupies about 0.5% of the animal's body volume. The eye's morphology suggests that it is extremely sensitive to light. The cornea of the dorsal eye is smooth with no dioptric apparatus. The retina consists of two wing-shaped lobes that are fused across the midline anteriorly. The rhabdomeral segments of the 7000 ommatidia form a compact layer of photosensitive membrane with an entrance aperture of more than 26 mm2. Within this layer, the volume density of rhabdom is more than 70%. Below the rhabdomeral segments, a thick layer of white diffusing cells scatters light upward into the photoreceptors. The arhabdomeral segments of the five to seven photoreceptors of each ommatidium are mere strands of cytoplasm that expand to accommodate the photoreceptor nuclei. The rhabdom is comprised of well-organized arrays of microvilli, each with a cytoskeletal core. The rhabdomeral segment cytoplasm contains mitochondria, but little else. The perikaryon contains a band of mitochondria, but has only small amounts of endoplasmic reticulum. There is no ultrastructural indication of photosensitive membrane cycling in these photoreceptors. Vestigial screening pigment cells and screening pigment granules within the photoreceptors are both restricted to the inner surface of the layer of the white diffusing cells. Below the retina, photoreceptor axons converge in a fan-shaped array to enter the dorsal surface of the brain. The eye's size and structure are consistent with a role for vision in shrimp living at abyssal hydrothermal vents.