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Photo ofStephen Macknik

Stephen L. Macknik, PhD

Professor of Ophthalmology, Neurology, and Physiology & Pharmacology

Tel: (718) 270-2972 • Fax: (718) 270-2972

e-mail: Stephen.Macknik@Downstate.edu

Background and Expertise:

My early vision research was on an intriguing illusion called backward masking, in which a visual target is rendered invisible by a masking stimulus presented 100 msec after the target is extinguished. It was as if the mask traveled back in time to destroy the target, before the brain could achieve conscious awareness of it. I employed a multidisciplinary approach that combined monkey electrophysiology, human psychophysics, and human fMRI to determine its neural mechanisms. I found that backward masking occurred when the mask inhibited the target's termination response–the response that occurs to the turning off of the target–about 100 msec after the stimulus is extinguished. So, once we realized that termination responses were critical to visibility, the mysterious timing of backward masking finally made sense: when the mask has just the right timing, it inhibits the target's termination response through classical lateral inhibition mechanisms. Without the termination response, the brain has a diminished signal from which to produce the percept of the target, and the target is therefore less visible. Previous work on neural coding in the brain had favored stimulus onset responses over termination responses. We published these studies, and follow up optical imaging studies of cortical activity, in Nature Neuroscience and PNAS. My colleagues in these studies were Margaret Livingstone, David Hubel, Susana Martinez-Conde, and Michael Haglund.

Because termination responses are critical to perception, one of the main questions to arise from this work was why the world appears visible even though it does not usually turn off. I realized that, indeed, the world does turn both on and off multiple times each second, from the point of view of individual neurons, due to eye movements. This prompted as series of studies on the effects of microsaccades on visual physiology and perception, on which I worked with Susana Martinez-Conde and David Hubel. We found that microsaccades drive bursting activity in the primary visual cortex of awake monkeys (Nature Neuroscience & PNAS) and perceptual transitions in humans (Neuron, Journal of Neuroscience, and Journal of Vision). Susana Martinez-Conde's and my laboratory have now begun to focus on the clinical ramifications of these results, and found that several neurological diseases, such as Parkinsonian disorders and Alzheimer's disease, have specific eye movement signatures that can help diagnose and track therapeutic interventions in patients. We received the EyeTrack Award for this work.

My lab went on to show, in collaboration with Peter Tse and Susana Martinez-Conde, with whole brain fMRI imaging in humans, the neural correlates of visual awareness of simple unattended targets. We found that neural circuits downstream of area V2, but within the occipital lobe, were sufficient to maintain visual awareness of this limited stimulus set. This study, published in PNAS in 2005, was the first to set an upper threshold for awareness of any stimulus within the visual hierarchy, which we achieved by controlling for our subjects' state of attention. Previous studies had not done this, and had therefore conflated circuits maintaining awareness with circuits that maintain attention. Studies in other labs (led by Assad, He, etc) have similarly shown that awareness is modular for moving targets or complex shapes in higher brain areas, when attention is controlled.

Working with Jose-Manuel Alonso, Harvey Swallow, and Susana Martinez-Conde, we then asked how the awake monkey primary visual cortex enhances attention at the center of the attentional focus and suppresses attention in the surround. Our experiments showed that a specific population of inhibitory neurons in the primary visual cortex–operating at the center of the attentional spotlight, no matter where it was positioned in the visual scene–suppressed the activity of a specific population of motion-direction selective neurons in the spotlight's surround. So the attentional spotlight does not enhance the spotlight's center so much as it inhibits noise from the surround from interfering with the responses in the center. This explained how one could enhance neuronal activity at the spotlight's center while also increasing signal-to-noise. The study was published in Nature Neuroscience in 2008, with several subsequent papers discussing further constraints of feedback in visual processing and attention.

Susana Martinez-Conde and I also studied the techniques of stage magicians, and sometimes their untested models of cognition, to discover the differential effects of smooth pursuit and saccadic eye movements on the spotlight of attention. These and other insights from our research into the neural bases of magic were published in Nature Reviews Neuroscience, Frontiers in Human Neuroscience, and PeerJ (where our study is the most downloaded paper in the journal).

Research Interests

My research focuses on three main lines of work:

  1. The neurobiology and perception of brightness and flicker
    Using human and monkey psychophysics and monkey physiology, we study the neural correlates of temporal contrast gain control in the brain. The state of the art in the study of temporal responses of neurons was the temporal impulse response function–which, when convolved with the stimulus's temporal profile, describes the neural response. But no previous research has accounted for termination responses in the temporal impulse response function. Our discoveries suggest that the temporal impulse response function should moreover vary as a function of stimulus duration. These findings could be critical to our understanding of contrast and brightness perception as a function of temporal lighting conditions.
  2. Abnormal blood flow in neurological and ophthalmological disease
    We develop advanced molecular imaging techniques for microscopic blood flow in neurological and ophthalmological diseases, specifically in epilepsy and age-related macular degeneration, but also in traumatic brain injury, which often results in both epilepsy and retinal degeneration.
  3. Attention and cognition in mental disease
    We investigate the neural link between attention, emotions, and autism, and mood disorders. People with autism have difficulty maintaining social relationships, and processing complex social information, especially in a real-time interactive setting. They also generally feature substantial comorbid mood disorders, which may well be related to their experienced difficulty in social interactions: depression and anxiety are nearly ubiquitous in people with autism. One pressing question is thus the extent to which negative mood due to depression and anxiety influences the ability of people with autism to process complex social information. Are they overwhelmed, experience difficulties with prioritizing attention, or do not appropriately engage other cognitive processes, in part because they concurrently experience a strongly negative emotional state? To test this, we measure, in collaboration with Profs. Ralph Adolphs of Caltech and Dan Kennedy of Indiana University, the ability of people with autism to allocate attention (through eye tracking and change detection measures), encode into memory (through subsequent questionnaire-based assessment), and process semantic depth (through subsequent structured interview) of complex social stimuli (film clips).
Education:
  • Graduate School: PhD, Harvard University (Margaret Livingstone, PhD)
  • Postdoctoral Fellowships: Harvard Medical School (David Hubel, MD)
    Cold Spring Harbor Laboratory (Zachary Mainen, PhD)
Selected Publications
  • Rieiro H., Martinez-Conde S., Macknik SL. (2013). "Casting Light On Previous Bumps in the Dark". Proceedings of the National Academy of Science (USA), doi/10.1073/pnas.1222875110.
  • Rieiro H, Martinez-Conde S, Macknik SL (2013). "Perceptual elements in Penn and Teller's "Cups and Balls" magic trick". PeerJ 1:e19 http://dx.doi.org/10.7717/peerj.19. * Featured publication, featured in Scientific American
  • Martinez-Conde S, Otero-Millan J, Macknik SL, (2013) "The impact of microsaccades on vision: towards a unified theory of saccadic function", Nature Reviews Neuroscience. 14: 83-96. *** Cover Article***
  • Rieiro H., Martinez-Conde S., Danielson AP, Pardo-Vazquez JL, Srivastava N, Macknik SL. (2012). "Optimizing the temporal dynamics of light to human perception." Proceedings of the National Academy of Science (USA) 102 (47):17178-17183. * Featured in Early Edition, NPR's Science Friday, LA Times, other media
  • Otero-Millan J, Serra A, Leigh RJ, Troncoso XG, Macknik SL, Martinez-Conde S (2011). "Distinctive features of saccadic intrusions and microsaccades in progressive supranuclear palsy". Journal of Neuroscience 31: 4379-4387. *Winner of the 2011 EyeTrack Prize–Tobii Technologies
  • Macknik SL, Martinez-Conde, S, Blakeslee S (2011) Sleights of Mind: What the Neuroscience of Magic Reveals About Our Everyday Deceptions, Henry Holt & Co.***Winner of Prisma Prize for Best Book of the Year. International Bestseller. Published or contracted in 20 languages and in > 100 countries, listed as one of the 36 Best Books of the Year by London's The Evening Standard . The bestselling science book in Spain for 6 weeks, peaking at #2 for all non-fiction for two weeks ***
  • Macknik SL, Martinez-Conde S (2009). "Real magic: future studies of magic should be grounded in neuroscience". Nature Reviews Neuroscience 10: 241.
  • Troncoso XG, Macknik SL, Otero-Millan J, Martinez-Conde S. (2008) "Microsaccades drive illusory motion in 'Enigma'". Proceedings of the National Academy of Science, 105:16033-16038; published ahead of print October 8, 2008, doi:10.1073/pnas.0709389105 (direct submission: Track II).
  • Macknik SL, King M, Randi J, Robbins A, Teller, Thompson J, Martinez-Conde S. (2008) "Attention and awareness in stage magic: turning tricks into research". Nature Reviews Neuroscience. advance online publication, 30 July 2008 | doi:10.1038/nrn2473 **** Featured in The New York Times, The Boston Globe, and National Public Radio***
  • Chen Y, Martinez-Conde S, Macknik SL, Bereshpolova Y, Swadlow HA, Alonso J-M. (2008) "Detection difficulty modulates neuronal activity in primary visual cortex". Nature Neuroscience, 11(8), 974-982. ***News and Views by John Reynolds (Nature Neuroscience 11(8): 861-862) – Recommended: Faculty of 1000***
  • Martinez-Conde S, Macknik SL, Troncoso XG, Dyar TA. (2006) "Microsaccades counteract visual fading during fixation", Neuron, 49, 297-305. ***Preview by Ralf Engbert (Neuron 49: 168-170). Recommended by the Faculty of 1000.***
  • Tse PU, Martinez-Conde S, Schlegel AA, Macknik SL, (2005), "Visibility and visual masking of simple targets are confined to areas in the occipital cortex beyond human V1/V2", Proceedings of the National Academy of Sciences (USA), 102 (47), pp.17178-17183.
  • Martinez-Conde S, Macknik SL, Hubel DH (2004), "The role of fixational eye movements in visual perception", Nature Reviews Neuroscience, 5, pp. 229-240. ***Featured Article of the Month.***
  • Martinez-Conde S, Macknik SL, Hubel DH., (2002), "The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex", Proceedings of the National Academy of Sciences (USA), 99(21), pp.13920-13925.
  • Macknik SL, Martinez-Conde S, Haglund MM, (2000), "The Role of Spatiotemporal Edges in Visibility and Visual Masking", Proceedings of the National Academy of Sciences (USA), 97(13), pp.7556-7560.
  • Martinez-Conde S, Macknik SL, Hubel DH, (2000), "Microsaccadic Eye Movements and Firing of Single Cells in Striate Cortex of Macaque Monkeys.", Nature Neuroscience, 3(3), pp.251-258.
  • Macknik SL, Haglund MM, (1999), "Optical Images of Visible and Invisible Percepts in the Primary Visual Cortex of Primates", Proceedings of the National Academy of Sciences (USA), 96(26), pp. 15208-15210.
  • Macknik SL, Livingstone MS, (1998), "Neuronal correlates of visibility and invisibility in the primate visual system", Nature Neuroscience, 1(2), pp. 144-149.