Michael J. Hawken

Cortical circuits and neuronal mechanisms of visual perception

My main research interest is defining the role of cortical neurons in visual processing. This work includes physiological and anatomical studies in the primate visual pathways, mainly the primary visual cortex. In conjunction with these physiological studies, I collaborate in studies that relate pursuit eye movements to perceptual performance.

Cortical Processing and Circuits: Much of my visual physiology work has centered on unraveling the cortical receptive field properties in adult monkey cortex. This is important for a number of reasons: visual cortex is one of the best understood cortical regions and appears to play a pivotal role in many of the features of visual analysis underlying visual perception. It is also strongly affected by deprivation and learning so having a solid understanding of the normal properties is essential to understanding dysfunction. My colleague, Andrew Parker, and I showed that the activity of individual neurons could match perceptual performance (Parker & Hawken, 1985; Barlow et al, 1987; Hawken & Parker, 1990) on a number of low-level visual tasks. With Andrew Parker while at Oxford and with my colleague Bob Shapley since I moved to NYU I have also studied how receptive fields are organized spatially (Hawken & Parker, 1987; Parker & Hawken, 1988; Hawken & Parker, 1991), and how different streams from the retina, the M and P-pathways, selectively influence the properties of different streams of cortical neurons (Hawken & Parker, 1984; Hawken et al, 1988), the temporal selectivity of cortical neurons (Hawken et al, 1996), the influence of surround suppression on receptive fields (Sceniak et al, 1999; 2001; 2002), organization of orientation selectivity (Ringach et al, 2002) and the chromatic organization of receptive fields (Johnson et al, 2001; 2004). From these latter studies we proposed a new view of chromatically double opponent receptive fields (Shapley & Hawken, 2002). Overall we have begun to build up a comprehensive picture of the complexity of receptive field organization in V1 and have developed a large database that we believe will offer important insights into cortical function.

In a related and complementary series of studies with Bob Shapley we have used techniques of reverse correlation that were developed by Dario Ringach when he was a student in our lab to investigate the mechanisms underlying receptive field organization (Ringach et al, 1997). From these studies (Ringach et al, 2003; Xing et al, 2004; 2005; 2006) we have proposed how excitatory and suppressive mechanisms are involved in the generation of orientation selectivity (Shapley et al, 2003) and spatial frequency tuning (Ringach et al, 2002; Xing et al, 2004).

Structure-Function Relationships in Primary Visual Cortex: On the one hand we often have detailed knowledge of neuronal firing to an array of visual stimuli, obtained from extracellular recording, that characterize the receptive field. On the other hand, from anatomical studies, we know about the intricate neuronal architecture and the patterns of synaptic connections both within V1 and between V1 and extra-striate cortex. In order to better understand such a complicated neuronal network, modeling how cortical neurons interact within the network is a crucial area of research. At present, there is one link that is missing that if found would enable much more realistic modeling of the cortex: the link between structure and function. In collaboration with Siddhartha Joshi I have recently developed a method called juxtacellular loose-patch (JC-LP) recording (Joshi & Hawken, 2006) to label neurons in primary visual cortex after functionally characterizing their receptive field properties. One of out goals is to identify subclasses of excitatory and inhibitory neurons and associate them with receptive field properties, thereby greatly extending our current knowledge of how the cortical circuits operate.

Modulation and Inhibition in Cortical Circuits: Primarily driven by recent work with a predoc and then postdoc in my lab, Anita Disney, I have begun to study how neurons in primary visual cortex are influenced by neuromodulators. It has been known for sometime that that there is an extensive innervation of cortex by cholinergic afferents, and the effects of ACh application to cortical neurons have shown mixed effects. Anita showed in her thesis work that one class of receptors for acetylcholine (ACh), the nicotinic receptors, are located on primary afferents arriving from the geniculate into layer 4c of monkey primary visual cortex. She hypothesized that nicotine should enhance geniculate transmission, and we devised a series of experiments to investigate this in vivo. We found that the response of neurons in layer 4c was enhanced by the iontophoretic application of nicotine, but neurons outside 4c were either unaffected or suppressed. Tantalizingly, the effects we observed are almost identical to those that are observed during an enhancement of response during attention in the awake-monkey, which prompted us to suggest that some of the effects of attention might be mediated by ACh via nicotinic receptors (Disney et al, 2007).

Most of the receptors for ACh on inhibitory interneurons are muscurinic so in future experiments we will test if there are effects of muscurinic agonists that mimic inhibitory or suppressive effects on tuning of cortical neurons. We have also started to use blockers of the inhibitory receptor, GABA, to determine whether the effects are mediated via enhanced inhibition in cortex. In addition, we have recently determined the distribution of neurons in primate V1 with the Kv3.1 and Kv3.2 ion channels that confer the fast-spiking phenotype on neurons, finding that in addition to the expected localization on sub-populations of inhibitory interneurons there is also expression on excitatory neurons (Constantinople et al, 2009). These results suggest that, unlike rodent cortex, primate cortex is likely to have a population of fast-spiking excitatory neurons.

Color and Motion Psychophysics and Eye Movements: In the 1980 s it was speculated that there were selective mechanisms for the perception of color and motion, and that these had their own separate pathways in the brain. In a series of psychophysical studies with Karl Gegenfurtner, started when he was a postdoc here at NYU and continued since he moved back to Germany, we found that stimuli that selectively isolate the chromatic pathway can provide signals to drive the perception of motion (Hawken et al, 1994; Gegenfurtner & Hawken, 1995; 1996; Hawken & Gegenfurtner, 1999).

Perception and action are intimately related. One intriguing question that has received a lot of attention recently is whether the same neural signals that are used to perceive visual objects are also used to initiate and maintain actions. In a study that formed his Ph.D. thesis I worked with Dario Ringach on recording vergence eye movements in response to a stimulus where the three-dimensional perception of depth comes from motion cues, but is not due to disparity (Ringach et al, 1996). In this study we found that the percept of motion in depth was strongly related to the vergence eye movements, suggesting that the same processing is used for perception as for driving motor action.

Another eye movement system that is particularly amenable to measurement is the pursuit system, it is voluntary and can be studied in the open loop phase. In a series of studies we sought to determine whether the motion signals that drive perception are the same as those that drive pursuit (Hawken & Gegenfurtner, 2001; Gegenfurtner et al, 2003; Spering et al, 2005; Braun et al, 2008) and, surprisingly, found that although they are strongly correlated they are not the same. These results suggest that, under some conditions, signals driving perception and action are distinct.

E-mail: mjh2@nyu.edu

Representative Publications

Ringach, D.L., Hawken, M.J. & Shapley R.M. (2002) Receptive field structure of neurons in monkey primary visual cortex revealed by stimulation with natural image sequences. Journal of Vision, 2, 12-24. pdf

Ringach, D.L., Bredfeldt, C.E., Shapley, R.M. & Hawken, M.J. (2002) Suppression of neural responses to non-optimal stimuli enhances tuning selectivity in macaque V1. Journal of Neurophysiology, 87, 1018-1027. pdf

Ringach, D.L., Shapley, R.M. & Hawken, M.J. (2002) Diversity and laminar specialization of orientation selectivity in macaque V1. Journal of Neuroscience, 22, 5639-5651. pdf

Shapley, R. & Hawken, M.J. (2002) Neural mechanisms for color perception in the primary visual cortex. Current Opinion in Neurobiology, 12, 426-432. pdf

Sceniak, M.P., Hawken, M.J. & Shapley, R.M. (2002) Contrast dependent changes in spatial frequency tuning: effects of a changing receptive field size. Journal of Neurophysiology, 88, 1363-1373. pdf

Ringach, D.L., Hawken, M.J. & Shapley, R.M. (2003) Dynamics of orientation tuning in macaque V1: the role of global and tuned suppression. Journal of Neurophysiology, 90, 342-352. pdf

Shapley, R.M., Hawken, M.J. & Ringach, D.L. (2003) Dynamics of orientation tuning in primary visual cortex and the importance of cortical inhibition. Neuron 38, 689-699. pdf

Kiorpes, L., Tang, C., Hawken, M.J. & Movshon, J.A. (2003) Ideal observer analysis of the development of spatial contrast sensitivity in macaque monkeys. Journal of Vision 3, 630-641. pdf

Gegenfurtner, K.R., Scott, B., Xing, D. & Hawken, M.J. (2003) A comparison of pursuit eye movements and perecptual performance in speed discrimination. Journal of Vision 3, 665-876. pdf

Johnson, E.N., Hawken, M.J. & Shapley, R.M. (2004) Cone inputs in macaque primary visual cortex. Journal of Neurophysiology 91, 2501-2514. pdf

Xing, D., Ringach, D.L., Shapley R.M. & Hawken M.J. (2004) Correlation of local and global orientation and spatial frequency tuning in macaque V1. Journal of Physiology 557, 923-933. pdf

Williams, P.E., Mechler, F., Gordon, J., Shapley, R.M. & Hawken, M.J. (2004) Entrainment to video displays in primary visual cortex of macaque and humans. Journal of Neuroscience 24: 8278-8288. pdf

Movshon, J.A., Kiorpes, L., Hawken, M.J. & Cavanaugh, J.R. (2005) Maturation of the macaque's lateral geniculate neurons. Journal of Neuroscience 25: 2112-2122. pdf

Xing, D., Shapley R.M., Hawken M.J. & Ringach, D.L. (2005) The effect of stimulus size on the dynamics of orientation selectivity in Macaque V1. Journal of Neurophysiology 94: 799-812. pdf

Spering, M., Kerzel, D., Braun, D.I., Hawken, M.J. & Gegenfurtner, K.R. (2005) Effects of contrast on smooth pursuit eye movements. Journal of Vision 5: 455-465. pdf

Joshi, S. & Hawken M.J. (2006) Loose-patch-juxtacellular recording in vivo-A method for functional characterization and labeling of neurons in macaque V1. Journal of Neuroscience Methods, 156, 37-49. pdf

Shapley, R.M, Hawken, M.J. & Xing, D. (2007) The dynamics of visual responses in primary visual cortex. Progress in Brain Research 165, 21-32. pdf

Disney, A.A., Aoki, C. & Hawken, M.J. (2007) Nicotinic receptors on thalamic afferents enhance visual responsiveness in macaque V1. Neuron 56, 701 - 713. pdf pdf_suppl

Johnson, E.B., Hawken, M.J. & Shapley R.M. (2008) Color and orientation selectivity in macaque V1. Journal of Neuroscience 28, 8096-8106. pdf

Braun, D.I., Mennie, N., Rasche, C., Hawken, M.J. & Gegenfurtner, K.R. (2008) Smooth pursuit eye movements to isoluminant targets. Journal of Neurophysiology 100, 1287-1300. pdf

Constantinople, C., Disney, A.A., Maffie, J., Rudy, B. & Hawken, M.J. (2009) A quantitative analysis of neurons with Kv3 potassium channel subunits Kv3.1b and Kv3.2 in macaque primary visual cortex. Journal of Comparative Neurology, 516, 291-311. pdf