Beyond the olfactory bulb: an odotopic map in the forebrain

Abstract

We report electrophysiological evidence that a simple odotopy, the spatial mapping of different odorants, is maintained above the level of the olfactory bulb (OB). Three classes of biologically relevant odorants for fish are processed in distinct regions of the forebrain (FB) in the channel catfish. Feeding cues, mainly amino acids and nucleotides, are represented in lateral, pallial portions of the FB, equivalent to the olfactory cortex of amniote vertebrates, whereas social signals mediated by bile salts are represented in medial FB centers, possibly homologous to portions of the amygdala. As in the OB, the different odorant classes map onto different territories; however, the response properties of units of the olfactory areas of the FB do not simply mirror those of the OB. For some units, distinctive response properties emerged, because the FB is the first center where odors subserving a common behavioral function (i.e., food function) converge.

Fig. 1.

Organization of the olfactory system and typical olfactory responses in the forebrain of the channel catfish. (A) Dorsal view of the front part of the head of a channel catfish dissected to reveal the FB, olfactory tract (OTr), and OE. Unit responses were recorded from the FB while odorant stimuli were presented by means of a constant flow of water passing across the OE. The EOG (data not shown) was recorded from the OE to monitor the onset of olfactory receptor responses while a microelectrode recorded responses of single FB neurons. Lighting highlights were reduced or eliminated from the figure by digital replacement with adjacent pixels. (B-F) Examples of odor responses of five different FB units are shown. Excitatory responses were obtained to mixtures (see Methods) of amino acids (B), bile salts (C), nucleotides (D), amino acids and nucleotides (E), and Arg and Met (F). All odorants shown were tested at 10^-5 M. (Time bar, 0.8 s.)

Fig. 2.

Schematic diagram showing odotopic representation in the dorsal OB (A) and the FB (B). Amino acid-responsive units are indicated by blue symbols, bile salt-responsive units are indicated in green, and nucleotide-responsive units are shown in red. Data for the OB were replotted from ref. . The points shown in B represent all of the units recorded and mapped in the present study. Electrode positions were plotted in Fig. 3 onto representative sections through key levels of the olfactory areas of the FB as indicated by the brackets and respective lettering.

Fig. 3.

Representative transverse sections from anterior (A) to posterior (D) through the FB of the channel catfish in which the olfactory tracts had been labeled by dextran-amine (orange-red shading) and counterstained for Nissl (purple-blue staining). The sections correspond to key areas of the olfactory terminal fields; levels of the sections (A-D) are indicated in the Inset below panel C and by the y value reflecting the relative antero-posterior distance from front to back of the FB. Plotted onto these sections are the electrode positions determined by the coordinate values (dots) or by reconstruction of lesions (X). The sites labeled 1B-F refer to locations where the respective recordings shown in Fig. 1B-F were obtained. Note the close correspondence between positions determined by coordinates and those from anatomical reconstructions. The color coding corresponds to that in Fig. 2. Complex units are indicated by lavender mtf. Medial terminal field; ptf, posterior terminal field; ltf, lateral terminal field.