Nonlocal Interactions in the Photoreceptor Transduction Process PETER HILLMAN, SHAUL HOCHSTEIN,and

BARUCH MINKE

From the Institute of Life Sciences, The Hebrew University, Jerusalem, Israel and the Department of Biological Sciences, Purdue University, West Lafayette, Indiana 47907

ABST R AC T We have recently demonstrated the dissection of the tra.nsduction process in the barnacle photoreceptor into antagonistic "excitor" and "inhibitor" processes. We now show that (a) the interaction between the two processes proceeds even when they are induced in different pigment molecules; (b) the excitor process appears to be slightly facilitated if those pigment molecules unaffected by the stimulus are in the stable metarhodopsin state or slightly inhibited if they are in the rhodopsin state; (c) there is a facilitatory interaction among the excitor processes induced in different pigment molecules. In case a, the interaction has a range of at least a few hundred angstroms, taking place in a time of less than a fraction of a second; in cases b and c, the range could be as little as "nearest neighbors" and the time as much as a few seconds. All these interactions could be intermediated by the "excitor" if it is a transmitter. INTRODUCTION

T h e mechanism o f transduction in p h o t o r e c e p t o r s is still unclear. Cone, 1973, a n d Yoshikami a n d Hagins, 1973, have p r o p o s e d an internal transmitter intervening between the photon-initiated p i g m e n t cascade a n d the c h a n g e in plasma m e m b r a n e c o n d u c t a n c e . O n e a p p r o a c h to the internal transmitter p r o b l e m is the spatial characterization o f some o f the processes involved: w h e t h e r or not there is a spread o f the influence o f these processes within the p h o t o r e c e p t o r cell. We have recently suggested the existence o f extrapigmental antagonistic "excitor" and "inhibitor" c o m p o n e n t s in the coupling o f the p i g m e n t cascade to the m e m b r a n e c o n d u c t a n c e c h a n g e in the p h o t o r e c e p t o r s o f the lateral ocelli o f the barnacle (Hillman et al., 1972; Hochstein et al., 1973) and the UV p h o t o r e ceptors o f the m e d i a n eyes ofLimulus (Minke et al., 1973b). In the barnacle (and presumably in Liraulus) the visual p i g m e n t has two thermally stable states, interconnected by a network o f thermally unstable states and thermal and phototransitions (Minke et al., 1974a). I n the barnacle, the stable states have absorption peaks at 532 and 495 nm, respectively (Hillman et al., 1972 and Minke et al., 1973a) and the excitor and inhibitor processes are activated by p h o t o n i n d u c e d transfer o f the p i g m e n t molecules f r o m the 532- to the 495-nm state a n d vice versa, respectively. Despite the lack o f direct evidence for the identification o f these states in this THE JOURNAL

OF G E N E R A L P H Y S I O L O G Y • V O L U M E 6 8 ,

1976

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THE JOURNAL

OF GENERAL PHYSIOLOGY

• VOLUME

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1976

preparation, Minke et al. (1973a and 1974a) suggested that the 532-nm state may be the rhodopsin state and the 495-nm state a metarhodopsin state (meta). Thus, net transfer of pigment from the rhodopsin to the meta state induces the excitor transduction process while reverse pigment transfer induces the inhibitor transduction process. The excitor process in isolation manifests itself in a prolonged depolarizing afterpotential (PDA) and the inhibitor process manifests itself in the depression or prevention of the PDA (anti-PDA). Saturating red stimulation (>600 nm) leaves nearly all of the pigment in the 495 meta state, while blue light (