Some things are so deeply culturally engrained that you can't see them - even if you are looking right at them. Architecture possesses an almost magical ability to be gigantic yet almost invisible. It can be imbued with tremendous political ideology, yet seem as innocent as the breeze.

From cave to skyscraper, architecture has an incredible ability to make the most bizarre of situations seem completely natural and normal. Staring at the skyline of a city, you can't help but wonder, in voice that sounds a little bit like David Byrne, 'How did we get here? And where exactly is here?'

The contemporary gallery is one of those places. A kind of bright, white blind spot at the heart of the culture industry. It's hard to imagine the world without those cool, smooth, almost empty, white gallery interiors. But it's important to remember that galleries haven't always been like that. It had to be invented.

The white cube as gallery space suggests both simplicity and innocence. But of course, this is really a kind of cloaking device disguising a tremendous cultural mechanism that confers values and meanings upon things within its gravity. If you rest your head against the cool smooth wall of a gallery, you can hear the cogs grinding.

The white cube is the result of a pact between high art and modernist architecture. A twentieth century invention, for twentieth century art. And its ingredients were the essential elements of modernist architecture: Whiteness and an abstract, primary solids. Art offered architecture the chance to indulge its tendency toward abstraction: The gallery program meant empty space, free of all that clutter that you need in buildings that people live or work in (its ironic that the functionalist credo of modernism excelled at the almost function-less program of gallery space).

Architectural abstraction meant buildings that resisted having direct meaning. This offered art the possibility of creating distance between itself and the real world.

The reality of buildings though, is that as soon as they leave the drawing board and become part of the world, they attract meaning like a magnet in a scrap yard.

Whiteness in architecture has a particular trajectory. It represented an absence of ornamentation. All that 19th century neo-classical decoration was seen as decadent, symbolic of the old order.

Mick Jagger sang 'No colors anymore I want them to turn black', unable to bear, in his heartbroken depression, the visual manifestation of happiness. Modernist architects felt the need to 'paint it white' because of architectures own painful recent history: the slums of the newly industrialised cities. Most of all, it meant the whitewashing of a history that had fist created and then failed the urban working class: a new beginning. White was the visual field of the tabula rasa.

Whiteness has a whole host of associations: of purity, of bridal virginity, of innocence. It also has the promise of as brand new stationary where all is yet to come.

The shape of the cube represents a similar desire to simplify, clarify and rationalise. Le Corbusier sat amongst the stones to the Acropolis sketching cubes, spheres and cones. It tends towards an idea rather than a thing. Things are awkward and messy. Things get dirty and damaged. Ideas stay perfect forever.

In the 19th century, the gallery and the artists studio were entirely different kinds of place. In the 20th century, these spaces converged.

The 19th gallery typology was descended from (or sometimes was converted from) a palace. Look at 19th century Gallery design, such as London's National Gallery or Tate Britain, and what you really see are buildings that should be filled with royal courts. Those endless sequences of rooms seem incomplete without layabout interbred members of the European aristocracy lounging on furniture. And of course, that is where art had previously resided: in the hallways of royalty. Galleries weren't white, they were other colours: you can buy Picture Gallery Red - from heritage paint company Farrow and Ball (which is based on the Picture Gallery at Attingham Park) or perhaps you might prefer Picture-Gallery Red (RL Number TH57) from the Ralph Lauren 'Thoroughbred' paint range.

The idea, or image of the gallery tells us about 19th century arts purpose. The 20th century gallery space had an entirely different approach. It began to appropriate the appearance of the artists studio, of un-ornamented industrial spaces. Partly as a democratic, partly asserting the growing importance of the artist as a cultural figure, as well as increasing arts immediacy. Of course, these new galleries weren't really industrial buildings. They just looked like them. Actually, they became increasingly refined: the planar abstract quality of the wall becoming more planar and more abstract by the use of the shadow gap - which articulates and separates the wall from the floor and ceiling. There is an unacknowledged perversity in the industrial aesthetic built with the craftsmanship of a palace.

The aesthetic of the gallery has spilled over into other areas. It's often hard to distinguish art space and boutique, between high-end dentist and restaurant. The gallery aesthetic which isolates objects, confers a non-specific seriousness, is everywhere. It's a tasteful, thoughtful, quiet way of presenting expensive products. It helps you forget that the objects are only products and suggests that they have something more about them.

Convergence between artists space and gallery space is illustrated by the Tate Modern. The appropriation of an old powerstation monumentalises the London art scene that preceded it. At Tate Modern, Herzog and de Muron have carefully preserved the industrial character, and have made almost unnoticeable interventions. They have made a kind of architecture that recalls semi-squatted unused old industrial spaces.

The show 'Can Buildings Curate' uses a series of projects by both artists and architects that explore attitudes towards the white cube. The last decade has seen bigger and bolder art gallery construction, a tendency beautifully illustrated by the inclusion of Zaha Hadids design for the Taiwanese Guggenheim (currently on ice, awaiting funding). It both outperforms Gehrys Bilbao in shape shifting but also through moving bits, sliding sections and elevating bits of building becomes a kind of hydraulic, anamatronic fair ground ride. The exhibition shows that there are other approaches that engage with the concept of the gallery space in an intelligent manner. Historically, it begins with exhibition designs: Duchamps '1200 Bags of Coal' (1938) and 'Mile of String' (1942); Friedrich Kieslers International Exhibition of New Theatre Technique (1938). These projects show the development of an attitude towards curation and display - making the act of looking into something active, something that needs to be negotiated. These pre-white cube projects are echoed in Goshka Macugas 'Cave' (1999) and Iceberg (2001). These create interiors suggesting natural phenomenons out of crumpled paper that are then hung with work by other artists. By making narrative places rather than white-cubed nowheres they challenge the orthodoxy of the neutral background. Conversely, the idea of the gallery as a terrible cultural prison is satirised by Davide Bertocchis 'Limo' (2003). A beautifully curved stretch limo spirals down the ramp of the Frank Lloyd Wrights Guggenheim. Round and round as it descends on the only journey it could possibly make. It reveals how deformed art has to be to make sense within the gallery. It suggests that the gallery is destined to produce artwork that will be ideally suited solely to its own unique qualities - rather than with relevance to the rest of the world.

Some of the architectural proposals included show demonstrate subtle and intelligent takes on the culture of the gallery building. The invisible mechanism of the gallery is explored in the Lucy Mackintosh Gallery Project (2005) by Decostered & Rahm. The design uses a network of hidden pipes to create different temperature zones within the interior volume. The infrastructure of heating is used instead of partitions to create zones within the space. Likewise, Sejima/Nishizawas 21st Century Museum of Contemporary Art makes a gallery space that plays with a lightness of architectural touch. Here, the gallery seems not quite there, a loose collection of almost-rooms and not-quite-corridors. Its architecture that's slight, suggestive and incredibly precise. It's almost as is the building is slipping away. It develops the abstraction and nothingness of the white wall into something spatial.

These kinds of projects play with the white cube as an architectural concept, extending and adjusting cultural conventions. It's an approach to the gallery echoes by OMA/AMOs concept work for St Petersburgs Hermitage. Tasked with looking into the future of the gallery, OMAs approach began with a stock taking of the existing spaces of the museum. Their approach suggested that the gallery itself was something that could be curated, and through the curation of the architecture, new meanings could be created.

These three projects show alternatives to the big gallery projects of the last ten years, epitomised by the Guggenheim Bilbao. Bilbao marks a particular moment in the history of the gallery. A moment where the gallery ballooned to gargantuan proportions, dwarfing and eclipsing its contents, and perhaps even the city that hosts it. For a moment it looked set to mushroom across the world - a franchised solution for cultural regeneneration.

But it seems to have proved a tipping point: rather than the beginning of the 21st century gallery, it's more likely to be a final flourish of the 20th century gallery. The relationship between business and art reached a kind of ultimate end game. Its business model required the host city to pay to use the Guggenheim brand with the museums then filled by a rotation of the foundation's huge art holdings. If this model hasn't exactly failed, it's certainly stalled.

Bilbao is an extraordinary display of architectural pyrotechnics. Many of the projects featured in 'Can Buildings Curate' suggest less explosive kinds of architecture. But kinds which engage with the cultural idea of the contemporary gallery space. Meaning rather than space becomes the raw material of architecture.

If anything, though, there remains a tasteful, cerebral atmosphere pervading these projects. The reality of modern galleries is an increasingly strange agglomeration of culture and entertainment, of culture and commerce, of restaurant, nightclub, and tourist destination. Architects - and perhaps even more, their high culture clients - perhaps need to accept and embrace that vulgar complexity of art spaces. Its high time they gave up their innocence and started to have some serious adult fun.