Primate Pupillary Light Reflex: Receptive Field Characteristics of Pretectal Luminance Neurons

2003 ◽  
Vol 89 (6) ◽  
pp. 3168-3178 ◽  
Author(s):  
Robert J. Clarke ◽  
Hongyu Zhang ◽  
Paul D. R. Gamlin

This study examined the response properties of luminance neurons found within the pretectal olivary nucleus (PON), which is the pretectal nucleus that mediates the primate pupillary light reflex. We recorded the activity of 121 single units in alert, behaving rhesus monkeys trained to fixate a back-projected laser spot while a luminance stimulus was presented. The change in the firing rate of luminance neurons was measured as a function of changes in the size, retinal illuminance, and position of the stimulus. We found that these neurons possessed large receptive fields, which were sufficiently distinct that they could be placed into three classes. Approximately 40% of the PON luminance neurons responded well to stimuli presented in either the contralateral or ipsilateral hemifield. These neurons were classified as “bilateral” neurons. In the primate, retinal projections to the pretectum and other retinorecipient nuclei are organized such that direct retinal input can only account for the contralateral hemifield responses of these neurons. Thus the representation of the ipsilateral hemifield in “bilateral” PON cells must result from input from a nonretinal source. Approximately 30% of PON neurons responded only to stimuli presented in the contralateral hemifield. These neurons were classified as “contralateral” neurons. Finally, approximately 30% of PON neurons responded to stimuli presented at or near the animal's fixation point. These neurons were classified as “macular” neurons. The mean firing rates of all classes of neurons increased with increases in stimulus size and luminance within their receptive fields. The thresholds and magnitude of these responses closely matched those that would be appropriate for mediating the pupillary light reflex. In summary, these results suggest that all three classes of PON neurons contribute to the behaviorally observed pupillomotor field characteristics in which stimuli at the macular produce substantially larger pupillary responses than more peripheral stimuli. The contributions of “bilateral” and “contralateral” cells account for pupillary responses evoked by peripheral changes in luminance, whereas the contributions of all three cell classes account for the larger pupillary responses evoked by stimuli in the central visual field.

2003 ◽  
Vol 89 (6) ◽  
pp. 3179-3189 ◽  
Author(s):  
Robert J. Clarke ◽  
Hongyu Zhang ◽  
Paul D. R. Gamlin

This study investigated the static and dynamic characteristics of the pupillary light reflex (PLR) in the alert rhesus monkey. Temporal characteristics of the PLR were investigated with Maxwellian viewing during sinusoidal changes in illumination of a 36° stimulus in both monkeys and humans. Bode plots of the PLR response were fitted by a linear model composed of a delay combined with a cascaded first- and second-order filter. The Bode magnitude plots conformed to this model with a sharp roll-off above 1.3 Hz for the human PLR and 1.9 Hz for the monkey PLR. Bode phase angle plots were fitted by this model with a delay of 280 ms for humans and 160 ms for monkeys. To investigate the influence of the sympathetic innervation of the iris on steady-state pupil diameter, dynamics of pupillary responses, and the latency of the PLR, we blocked this innervation pharmacologically with a selective alpha-1 adrenoreceptor antagonist. Although there was a resultant miosis (decrease in pupil diameter) from the relaxation of the pupil dilator muscle, no other measures of the PLR, including the dynamics and latency, were significantly affected by this treatment. We examined the pupillary responses evoked by visual stimuli presented either binocularly or monocularly at various locations on a 80 × 60° tangent screen. These pupillomotor fields revealed that, as has been reported for humans, stimuli at the fovea and surrounding macular region of monkeys produce substantially larger pupillary responses than more peripheral stimuli and that binocular responses are substantially greater than can be accounted for by the linear summation of binocular retinal illuminance. In conclusion, we found that the spatial characteristics of the PLR of the rhesus monkey are very similar, in all important aspects, to those reported for humans and that the temporal responses of the PLR are comparable between the two species. The rhesus monkey thus provides an excellent model for experimental studies of the neural control of the pupil.


2009 ◽  
Vol 1 (1) ◽  
pp. 19 ◽  
Author(s):  
Wolfgang H. Zangemeister ◽  
Thilo Gronow ◽  
Ulrich Grzyska

We examined effects of diabetes mellitus (DM) on the pupillary light reflex (PLR). Phasic pupillary response to a single light stimulus (200 ms) (pPLR) and to continuous sinusoidal stimuli with four different frequencies (0.1, 0.3, 0.7, 1.3Hz) (cPLR) were examined in 52 DM patients and 21 control subjects. We asked: does recording and frequency analysis of cPLR together with short time fourier [STFT] analysis of pPLR differentiate better between DM patients and normal subjects than pPLR only? Initial pupil diameter was significantly decreased in the DM group. For pPLR. maximal contraction velocity (Vmax), Vmax of redilation 1, reflex-amplitude and pPLR latency were significantly reduced in those patients who also showed signs of diabetic autonomic neuropathy (DNP). Tests of dynamic pupillary light reflex (cPLR) revealed that all DM patients had a significantly reduced gain at lower frequencies. Pupil phase lag was greater at 0.1 and 0.3Hz and smaller at 0.7 and 1.3 Hz in the DNP group (p<0.001). Comparison of single pPLR recordings of 5 DNP patients with 5 subjects using short time fast fourier (STFT) analysis revealed a characteristic change from low frequency content in healthy subjects to high frequency content in DNP patients. Significant changes in the PLR in DM can be found only when symptoms of autonomic neuropathy have been shown. Both sympathetic and the parasympathetic nervous systems are affected by diabetic autonomic neuropathy. Only recording of cPLR , together with STFT of pPLR can identify significant pathological deficits of pupillary control in single cases.


2019 ◽  
Vol 225 (1) ◽  
pp. 403-425 ◽  
Author(s):  
Paul J. May ◽  
Wensi Sun ◽  
Nicholas F. Wright ◽  
Jonathan T. Erichsen

AbstractThe motor outflow for the pupillary light reflex originates in the preganglionic motoneuron subdivision of the Edinger–Westphal nucleus (EWpg), which also mediates lens accommodation. Despite their importance for vision, the morphology, ultrastructure and luminance-related inputs of these motoneurons have not been fully described in primates. In macaque monkeys, we labeled EWpg motoneurons from ciliary ganglion and orbital injections. Both approaches indicated preganglionic motoneurons occupy an EWpg organized as a unitary, ipsilateral cell column. When tracers were placed in the pretectal complex, labeled terminals targeted the ipsilateral EWpg and reached contralateral EWpg by crossing both above and below the cerebral aqueduct. They also terminated in the lateral visceral column, a ventrolateral periaqueductal gray region containing neurons projecting to the contralateral pretectum. Combining olivary pretectal and ciliary ganglion injections to determine whether a direct pupillary light reflex projection is present revealed a labeled motoneuron subpopulation that displayed close associations with labeled pretectal terminal boutons. Ultrastructurally, this subpopulation received synaptic contacts from labeled pretectal terminals that contained numerous clear spherical vesicles, suggesting excitation, and scattered dense-core vesicles, suggesting peptidergic co-transmitters. A variety of axon terminal classes, some of which may serve the near response, synapsed on preganglionic motoneurons. Quantitative analysis indicated that pupillary motoneurons receive more inhibitory inputs than lens motoneurons. To summarize, the pupillary light reflex circuit utilizes a monosynaptic, excitatory, bilateral pretectal projection to a distinct subpopulation of EWpg motoneurons. Furthermore, the interconnections between the lateral visceral column and olivary pretectal nucleus may provide pretectal cells with bilateral retinal fields.


2000 ◽  
Vol 84 (2) ◽  
pp. 953-963 ◽  
Author(s):  
Milton Pong ◽  
Albert F. Fuchs

To investigate whether the simian light reflex is a reasonable model for the human light reflex, we elicited pupillary responses in three behaving rhesus macaques. We measured the change in pupillary area in response to brief (100 ms), intermediate (1 s), and long (3–5 s) light flashes delivered by light-emitting diodes while the monkey fixated a stationary target. Individual responses in the same monkey to either 100-ms or 1-s stimuli of the same light intensity were quite variable. Nevertheless, in response to the 100-ms stimulus, average pupillary constriction and peak constriction velocity increased and latency decreased linearly with the log of stimulus luminance. The minimum average constriction latency across monkeys for the brightest flash was 136 ms. A linear decrease of constriction latency with stimulus luminance also occurs in humans, but their latencies are ∼70 ms longer. In addition, peak constriction velocity was highly correlated with the decrease in pupillary area. Dilation metrics were not as well related to stimulus luminance as were constriction metrics. The latency from flash offset to the onset of dilation was relatively constant, averaging ∼480 ms. Peak dilation velocity was also correlated, but less well, with the increase in pupillary area. Constriction generally was greater and of longer duration for 1-s light pulses than for 100-ms pulses of equal luminance. The initial time courses of the responses to the two stimuli of different durations were identical until ∼150 ms after response onset. Human pupillary responses for long and short flashes also have identical initial time courses. For very long (3–5 s) and very bright constant-luminance stimuli, the simian pupil underwent oscillations at frequencies of 0.9–1.6 Hz. Similar oscillations, called hippus, occur in the human pupillary light reflex. Like humans, the monkeys also exhibited consensual and binocular pupillary responses. Except for response latency, the pupillary responses in the two primate species are otherwise quite similar. Therefore any knowledge we gain about the neuronal substrate of the simian light reflex can be expected to have considerable relevance when extrapolated to humans.


2020 ◽  
Vol 8 (4_suppl3) ◽  
pp. 2325967120S0027
Author(s):  
Olivia E. Podolak ◽  
Kristy B. Arbogast ◽  
Joshi B. Nabin ◽  
Kenneth Ciuffreda ◽  
Matthew Grady ◽  
...  

Background: Despite advancements, concussion diagnosis remains reliant on subjective symptom report and clinical assessments. Visual deficits and autonomic dysfunction have been described following concussion. Testing of the pupillary light reflex (PLR) is a simple, portable, non-invasive, and objective means of quantifying pupillary function. Purpose: The aim of this study was to objectively evaluate pupillary responses to a light stimulus in concussed adolescent athletes and to determine whether clinical assessments correlated with PLR responses after a diagnosed concussion when compared to pre-injury responses. Methods: In this prospective cohort study, PLR and clinical measures [PCSI and/or SCAT symptom scales, near point of convergence (NPC) and accommodation amplitude (AA) of both eyes] were assessed in 93 (45 female), non-concussed adolescent athletes (ages 14-18) during their pre-season. PLR was obtained in response to a brief white light stimulus using a hand-held pupillometer. During each assessment, three monocular trials were performed in each eye alternatively, with subsequent averaged responses for each eye. Seven athletes (ages 14-17) sustained a concussion and had post-injury assessments of PLR and clinical measures completed longitudinally through recovery. Results: All seven concussed athletes completed PLR and clinical assessments at least once post-injury (mean initial day of evaluation = 6 days post injury). Six out of the seven concussed athletes demonstrated an increase in steady state diameter of 24% (median 18%), minimum pupil diameter of 17% (median 11%) and a maximum constriction velocity of 28% (median 33%) following concussion which decreased over the course of recovery, returning to pre-injury or below pre-injury measurements. Six of seven of the concussed athletes completed NPC and AA assessments at both pre-season and post-injury timepoints. In contrast to the PLR findings, both NPC and AA measures were normal at post-injury assessments. Reported symptom scores improved throughout recovery, correlating with PLR response recovery, with both returning to pre-injury measurements. Conclusion: Pupil responsivity was found to be significantly enhanced after concussion compared to pre-injury measurements, waning over time during recovery, following a similar trajectory as symptom burden. NPC and AA, which have autonomic contributions and are clinical measures, were normal pre- and post-injury and did not differentiate the concussed state from the uninjured state in our series. Our preliminary results demonstrate that dynamic PLR responses may detect acute autonomic deficits that are not evident via clinical assessments. Further investigation of its potential utility as sensitive and objective biomarker in concussion diagnosis, management and sports clearance is warranted.


Sign in / Sign up

Export Citation Format

Share Document