Ocular dominance columns were important in early studies of
cortical plasticity, as it was found that
monocular deprivation causes the columns to degrade, with the non-deprived eye assuming control of more of the cortical
cells.[3]
It is believed that ocular dominance columns must be important in
binocular vision. Surprisingly, however, many
squirrel monkeys either lack or partially lack ocular dominance columns, which would not be expected if they are useful. This has led some to question whether they serve a
purpose, or are just a
byproduct of development.[4]
History
Discovery
Ocular dominance columns were discovered in the 1960s by
Hubel and
Wiesel as part of their
Nobel prize winning work on the structure of the visual cortex in
cats. Ocular dominance columns have since been found in many animals, such as
ferrets,
macaques, and
humans.[2] Notably, they are also absent in many animals with
binocular vision, such as
rats.[5]
Structure
A
simulation of the ocular dominance column
pattern, as might be seen if the surface of
V1 were colored according to eye preference.A typical
map of the relationship between ocular dominance,
orientation, and
cytochrome oxidase. Dark and light areas represent
neurons that respond
preferentially to the left and right eye. Colors represent orientation selectivity[note 1] of the neurons. Areas outlined in white have high levels of
cytochrome oxidase (function not yet established).[4] Notice that the centers of orientation "
pinwheels" and cytochrome oxidase blobs both tend to be in line with the centers of the ocular dominance columns, but there is no obvious relation between orientation and cytochrome oxidase.
Ocular dominance
columns are stripe shaped regions of the
primary visual cortex that lie perpendicular to the orientation columns,[6] as can be seen in the accompanying figure. Different species have somewhat different morphologies and levels of organization. For example,
humans,
cats,
ferrets, and
macaques all have fairly well defined columns, while
squirrel monkeys have quite
variable columns. There is even variation in expression in individuals of the same
species and in different parts of the cortex of the same individual.[4][7]
The columns are
innervated by input from the
lateral geniculate nucleus (LGN) into
cortical layer 4 and have mostly
reciprocal projections to many other parts of the visual cortex.[8]
Relation to other features of V1
The ocular dominance
columns cover the
primary (striate) visual cortex, with the exception of
monocular regions of the
cortical mapcorresponding to
peripheral vision and the
blind spot.[7] If the columns corresponding to one eye were colored, a pattern similar to that shown in the accompanying figure would be visible when looking at the
surface of the cortex. However, the same region of cortex could also be colored by the direction of
edge that it responds to, resulting in the
orientation columns, which are laid out in a characteristic
pinwheel shape.[note 2] Similarly, there are columns in the cortex that have high levels of the protein
cytochrome oxidase. These are called cytochrome oxidase "
blobs" because of their scattered blob-like appearance.
All three types of
column are present in the
visual cortex of humans[4] and macaques,[6] among other animals. In macaques, it was found that both blobs and pinwheel centers tend to lie in the center of ocular dominance columns,[6] but no particular relation has been found between pinwheel centers and blobs.[6] In humans, the
layout of the columns is similar; however, humans have somewhat variable column expression with at least one subject having disordered columns similar to those commonly found in squirrel monkeys.[7]
Most early
models of the columns supposed that there were
discrete "modules" or "
hypercolumns"
tiling the cortex, consisting of a
repeating unit containing a full set of
orientation and ocular dominance columns. While such units can be constructed, the map of columns is so distorted that there is
no repeating structure and no clear boundaries between modules.[6] Additionally, practically every combination of having or not having orientation, dominance, and
cytochrome oxidase columns has been observed in one
species or another.[4] Further confusing the issue,
squirrel monkeys don't always express columns, and even when they do the cytochrome oxidase blobs are not in
register with the ocular dominance columns.[9]
Development
Formation
There is no
consensus yet as to how ocular dominance
columns are initially
developed. One possibility is that they develop through
Hebbian learning triggered by
spontaneous activity coming from
retinal waves in the
eyes of the developing
fetus, or from the
LGN. Another possibility is that
axonal guidance cues may guide the formation, or a combination of mechanisms may be at work. It is known that ocular dominance columns develop
before birth, which indicates that if an activity dependent mechanism is involved it must work based on
intrinsic activity rather than being
sensory experience dependent.[10] It is known that
spontaneouswaves of activity in the
retina occur before birth and that these waves are crucial for eye specific segregation of inputs to the LGN by correlating the activity of nearby neurons.[11] Similarly, the
correlated activation for the retinal waves may direct development of the ocular dominance columns, which receive input from the LGN.[12] Similar spontaneous activity in the cortex may also play a role.[12][13] In any case, it has been shown that disrupting the retinal waves at least alters the pattern of ocular dominance columns.[12]
Plasticity
Sensitive periods
Although the ocular dominance
columns are formed before birth, there is a period after birth—formerly called a "
critical period" and now called a "
sensitive period"—when the ocular dominance columns may be modified by
activity dependent plasticity. This plasticity is so strong that if the signals from both eyes are blocked the ocular dominance columns will completely
desegregate.[14] Similarly, if one eye is closed ("
monocular deprivation"),[3] removed[15]("
enucleation"), or
silenced[16] during the sensitive period, the size of the columns corresponding to the removed eye shrink dramatically.
Models
Many models have been proposed to explain the development and
plasticity of the ocular dominance columns. In general these models can be split into two categories, those that posit formation via
chemotaxis and those that posit a
Hebbian activity dependent mechanism.[12] Generally, chemotaxis models assume activity independent formation via the action of
axon guidance molecules, with the structures only later being refined by activity, but there are now known to be activity dependent [17][18] and activity modifying [19][20] guidance molecules.
Modified Hebbian learning
One major model of the formation of the stripes seen in ocular dominance
columns is that they form by
Hebbiancompetition between axon terminals.[21]
The ocular dominance columns look like
Turing patterns, which can be formed by modified Hebbian mechanisms. In a normal
Hebbian model, if two neurons are connected to a neuron and fire together, they increase the strength of the synapses, "moving"[note 3][22] the
axon terminals closer together. The model must be modified to incorporate incoming activity that is locally excitatory and long range inhibitory, because if this is not done then the column width will only be dependent on the width of the axonal arbor, and also segregation will often fail in the presence of inter eye correlation.[21] This basic model has since been extended to be more physiologically plausible with the addition of
long term potentiation and
depression,
synaptic normalization,[23]neurotrophin release,[24]reuptake,[25] and
spike-timing-dependent plasticity.[26]
Chemotaxis
Chemotactic models posit the existence of
axon guidance molecules that direct the initial formation of the ocular dominance columns. These molecules would guide the axons as they
develop based on markers specific to the
axons from each eye.[12] All chemotactic models must take into account the activity dependent effects demonstrated in later development,[27] but they have been called for because several pieces of evidence make entirely activity dependent formation unlikely. First, it has been shown that the ocular dominance columns in squirrel monkeys have mirror symmetry across the cortex. This is very unlikely to occur by activity dependent means because it implies a correlation between the nasal[note 4]retina of one eye and the temporal[note 5] retina of the other, which has not been observed. Furthermore, work in achiasmatic[note 6]Belgian sheepdogs has shown that columns can form between the projections from the temporal and nasal retina of the same eye, clearly suggesting a nasal-temporal labeling, rather than
contralateral vs.
ipsilateral, which would be much easier to explain with activity dependent mechanisms.[28] Despite this, a molecular label that directs the formation of the ocular dominance columns has never been found.[12]
Function
It has long been believed that ocular dominance columns play some role in
binocular vision.[12] Another candidate function for ocular dominance columns (and for columns in general) is the minimization of connection lengths and processing time, which could be evolutionarily important.[29] It has even been suggested that the ocular dominance columns serve no function.[4]
Notes
^This means, for example, that neurons in the areas marked in red fire more when a vertical
edge is visible, green when a horizontal edge is visible, orange when 45°, etc.
^A very good analogy for this is the idea of coloring a map. Just like a map of
Asia could be colored by religion or by language, the columns are not physical things but regions defined by shared attributes. Also much like a map of religion the borders tend to be fuzzy with no clear distinction between one area and the next columns often don't have sharp borders. Similarly, there may be overlap, just as people at the border between
France and
Germany are a mixture of French speakers, German speakers, or
bilingual. There are even occasional neurons belonging to the
ipsilateral eye in a
contralateral column just like the occasional
Portuguese speaker may be found in
China. It was once believed the columns were discrete units with sharp borders but the idea of fuzzy, mostly continuous regions is now preferred.
^The axon terminals don't actually move, but they grow in size and number according to level of activity, the net result being that the output from any particular neuron moves as it loses connection to one neuron and gains connection to another.
^Adams, Daniel L.; Horton, Jonathan C. (2003). "Capricious expression of cortical columns in the primate brain". Nature Neuroscience. 6 (2): 113–114.
doi:
10.1038/nn1004.
PMID12536211.
S2CID8394582.
^Hocking, Davina R.; Horton, Jonathan C. (1998). "Effect of early monocular enucleation upon ocular dominance columns and cytochrome oxidase activity in monkey and human visual cortex". Visual Neuroscience. 15 (2): 289–303.
doi:
10.1017/S0952523898152124.
PMID9605530.
S2CID19011361.