Visual Neuroscience



Photoreceptor inner segments in monkey and human retina: Mitochondrial density, optics, and regional variation


Q.V.  HOANG  a1 a4, R.A.  LINSENMEIER  a1 a2 a3 c1, C.K.  CHUNG  a1 and C.A.  CURCIO  a5
a1 Department of Biomedical Engineering, Northwestern University, Evanston
a2 Department of Neurobiology and Physiology, Northwestern University, Evanston
a3 The Institute for Neuroscience, Northwestern University, Evanston
a4 Integrated Science Program, Northwestern University, Evanston
a5 Department of Ophthalmology, University of Alabama, Birmingham

Abstract

The present work quantifies aspects of photoreceptor structure related to mitochondria, inner segment dimensions, and optical properties, as a basis for furthering our understanding of rod and cone function. Electron-microscopic analyses were performed on the retina of one stumptail macaque (Macaca arctoides) to obtain stereological measurements of ellipsoid mitochondrial density, and sizes and shapes of outer and inner segments. In addition, the distribution of mitochondria and the optical properties of human foveal cones were examined with electron microscopy and Nomarski differential interference contrast (NDIC) imaging. Mitochondria comprised 74–85% of cone ellipsoids and 54–66% of rod ellipsoids in macaque. Ellipsoid volume increased with eccentricity by 2.4-fold for rods and more than 6-fold for cones over eccentricities to 12.75 mm, while the volume of the outer segment supported by the ellipsoid was essentially constant for both rods and cones. Per unit volume of outer segment, cones contained ten times as much mitochondria as rods. In human fovea, as in the rest of the retina, most cone mitochondria were located in the distal inner segment. In the foveal center, however, there are also mitochondria in the myoid, as well as in the outer fiber, proximal to the external limiting membrane (ELM). Analyses of the optical aperture of human foveal cones, the point at which their refractive index clearly differs from the extrareceptoral space, showed that it correlated well with the location of mitochondria, except in the foveal center, where the aperture appeared proximal to the ELM. While mitochondria have an important metabolic function, we suggest that the striking differences between rods and cones in mitochondrial content are unlikely to be determined by metabolic demand alone. The numerous cone mitochondria may enhance the waveguide properties of cones, particularly in the periphery.

(Received July 9 2001)
(Accepted May 17 2002)


Key Words: Photoreceptor; Retina; Mitochondria; Retinal metabolism; Photoreceptor optics.

Correspondence:
c1 Address correspondence and reprint requests to: Robert A. Linsenmeier, Biomedical Engineering Department, Northwestern University, 2145 Sheridan Rd., Evanston, IL 60208-3107, USA. E-mail: r-linsenmeier@northwestern.edu