Further study of the control of place cell firing by intra-apparatus objects

The angular positions of hippocampal place cell firing fields are accurately controlled by the position of a single salient cue card attached to the wall of a recording cylinder; when the card is rotated, fields rotate equally. In contrast, the control exerted by 3-dimensional objects placed directly in the recording arena depends on their arrangement. When three objects lie on the vertices of an isosceles triangle near the center of the cylinder they rarely exert any control over the angular positions of firing fields. However, if the isosceles triangle is dilated so that its vertices are against the apparatus wall, the objects exert virtually ideal control over angular field position. Why do the objects gain control when they are against the cylinder wall? One possibility is that the asymmetry in the object set is more easily detected when the objects are far apart so that they provide a better polarizing cue. This hypothesis assumes that the identity of individual landmarks is not recognized by the place cell system whereas their geometric arrangement provides crucial information for controlling place field positions. If this is true, putting the 3 objects against the cylinder wall on the vertices of an equilateral triangle should cause a loss of stimulus control over the angular positions of firing fields. To the contrary, we found that the firing fields of most place cells (23/29) were accurately controlled by the equilateral object arrangement. Moreover, 5/6 of the uncontrolled cells were in a single animal. These results bolster our previous suggestion that the centrally placed objects fail to control place field positions because the computations necessary to form a stable reference frame are very difficult when the animal can go between stimuli.